Reference Work Entry

Handbook of Paleoanthropology

pp 1441-1481

Date:

4 Role of Environmental Stimuli in Hominid Origins

  • Elisabeth S. Vrba

Abstract

Environmental stimuli have influenced the evolution of hominids and other mammals at the levels of ontogeny, organismal adaptation, and speciation. I review some agreement which has emerged— as well as persistent debates— on the issue of environmental linkages to hominid adaptation. I discuss some current hypotheses which link physical change, adaptation, and speciation in general and in hominids in particular (including hypotheses on the role of ecological specialization and generalization, the coordinated stasis and variability selection hypotheses, habitat theory and the turnover pulse hypothesis); and revisit some persistent debates (such as on whether or not there was mammalian species’ turnover in the Turkana Basin during the Plio-Pleistocene). The relation of hominid evolution to the recent finding of several turnover pulses coincident with global cooling trends in the 10-Ma Recent record of all African larger mammals is considered. One example of hypotheses which address issues of environmental stimuli of ontogenetic evolution is the heterochrony pulse hypothesis: the generative properties shared among lineages can result not only in coherence of morphological changes but also in a strongly nonrandom timing of heterochrony events, as diverse lineages respond in parallel by similar kinds of heterochrony to the same environmental changes. I give some mammalian and hominid examples involving body enlargement by prolongation of growth, and attendant “shuffling” of body proportions including relative increase in brain volume, namely encephalization.

Abstract

Environmental stimuli have influenced the evolution of hominids and other mammals at the levels of ontogeny, organismal adaptation, and speciation. I review some agreement which has emerged— as well as persistent debates— on the issue of environmental linkages to hominid adaptation. I discuss some current hypotheses which link physical change, adaptation, and speciation in general and in hominids in particular (including hypotheses on the role of ecological specialization and generalization, the coordinated stasis and variability selection hypotheses, habitat theory and the turnover pulse hypothesis); and revisit some persistent debates (such as on whether or not there was mammalian species’ turnover in the Turkana Basin during the Plio-Pleistocene). The relation of hominid evolution to the recent finding of several turnover pulses coincident with global cooling trends in the 10-Ma Recent record of all African larger mammals is considered. One example of hypotheses which address issues of environmental stimuli of ontogenetic evolution is the heterochrony pulse hypothesis: the generative properties shared among lineages can result not only in coherence of morphological changes but also in a strongly nonrandom timing of heterochrony events, as diverse lineages respond in parallel by similar kinds of heterochrony to the same environmental changes. I give some mammalian and hominid examples involving body enlargement by prolongation of growth, and attendant “shuffling” of body proportions including relative increase in brain volume, namely encephalization.

4.1 Introduction

It is a truism that environmental stimuli have influenced the evolution of hominids and all other life forms. The challenge is to understand the causal subcategories: what are the hypotheses and predictions that should be tested, and what kinds of data can be used to best effect? My approach is based on three premises: (1) we need to study not only the hominids but also their wider biotic and environmental context; (2) given the aim to understand hominid evolution, the theory of evolution should be accorded more prominence than has been the norm; and an expanded theoretical framework is needed. A focus on the dynamics which link the environment to selection and adaptation at the organismal level is insufficient. One also needs to consider the causal linkages from the environment to dynamics at lower and higher levels—from morphogenesis during organismal ontogeny to the macroevolutionary level of species turnover (speciation and extinction)—and investigate the separate and combined roles in the origins of new phenotypes and species; and (3) the direct influence of physical environmental stimuli on evolution at each level deserves more intensive study than it has been accorded traditionally. For much of the century following Darwin (1859), the research disciplines of geology (including climatology) and evolutionary paleontology were conducted separately. Speculations abounded on how they might link, but analyses directly integrating data from both areas remained sparse. This changed over the past 40–50 years as more refined methods led to discovery of new patterns and causal principles in paleoclimatology (e.g., the astronomical climatic cycles [Hays et al. 1976]) and in the fossil record (e.g., rigorous phylogenetic hypotheses, geochemical inference of past diet, etc.). Early papers linking evidence of physical change with hominid evolution concerned particular stratigraphic sequences in South and East Africa (respectively Vrba 1974, 1975; Coppens 1975; both compared climatic indications from mammalian change with the hominid record), the circum-Mediterranean area (Hsü et al. [1977] implicated the Messinian Salinity Crisis in hominid origin), and comparison of global climatic data with the hominid record (Brain 1981).

Darwin (1859) argued that the initiating causes of phenotypic change and speciation are located at the level of organisms, namely natural selection, particularly arising from competition: “… each new species is produced … by having some advantage over those with which it comes into competition …” (p 320). He stressed climatic effects on competition rather than on population structure: “in so far as climate chiefly acts in reducing food, it brings on the most severe struggle between the individuals … .” (p 68). Darwin thought that an understanding of organismal\selection and adaptation will also answer the question of species’ origins. Most later evolutionary studies, including those in paleoanthropology, have continued in this tradition. (See Tattersall [1997a] who argued that “paleoanthropology fell completely under the sway of the evolutionary views of the [neoDarwinian] Synthesis—where it remains, for the most part, today.”) The questions I will address, using theory and evidence, include how physical dynamics have influenced species’ structure and speciation, organismal ontogenetic systems, and selection and adaptation. I also consider some of the interactions among these levels.

“Hominidae” is here understood in the traditional sense (Howell 1978) to exclude Pan and Gorilla. I use the term “species” for a sexually reproducing lineage, the members of which share a common fertilization system; and “speciation” for the divergence of the fertilization system in a daughter population to reproductive isolation from the parent species (Paterson 1982), with awareness of the difficulties involved in applying such concepts to the fossil record (Kimbel 1991; Vrba 1995a). The terms “habitat” and “habitat-specificity” of an organism or species refer to the set of resources that are necessary for life; resources are any components of the environment that can be used by an organism in its metabolism and activities, including temperature, relative humidity and water availability, substrate characteristics, places for living and sheltering, all kinds of organic foods, such as plants and prey, mates, and other mutualist organisms in the same or different species (Vrba 1992). An organism's biotic environment derives from other organisms and biotic interactions such as competition, parasitism, predation, and mutualism. “Physical change” refers to the global and local effects from extraterrestrial sources, including the astronomical climatic cycles, and from dynamics in the earth's crust and deeper layers as manifested by topographic changes such as rifting, uplift, sea level change, and volcanism.

4.2 Physical change, adaptation, speciation: some current hypotheses

The traditional hypothesis follows Darwin closely and has often been called neo-Darwinian. In its most conservative form, it assumes that adaptation and speciation are always driven by natural selection. The particular causes of selection are seen as very diverse, the most important being organismal interactions—such as competition and predation—that can act alone, or in combination with physical change, to initiate and complete speciation (and extinction). Under this null hypothesis, H 0, selection pressures that cause speciation differ from group to group and from one local area to the next. To explore how this model's predictions differ from others, let us ask: what rhythm of speciation events would we expect if we could see all the events in the real world across the entire area under study (e.g., Africa) and if we plotted their frequencies against time? H 0 predicts that the pattern of origination frequencies for large areas, over long time, is a random walk in time with an averagely constant probability of origination. Examples of such arguments are found in Van Valen (1973), Hoffman (1989), McKee (1993), and Foley (1994). In contrast, a number of hypotheses share the argument that physical change is required for initiation of turnover, with the consequent prediction that speciation and extinction frequencies should be nonrandomly distributed in time in association with episodes of physical change. I will discuss several such hypotheses after introducing some relevant theory.

4.2.1 Allopatric speciation

Allopatic speciation occurs in isolated populations that have been separated by vicariance or by dispersal over barriers. (Vicariance is the fragmentation of a formerly continuous species’ distribution into separated populations.) Gulick (1872), who studied the Hawaiian fauna, was the first to argue that the causes of speciation are not well explained by selection among competitors but that vicariance brought about by physical changes was seminal in initiating speciation. Mayr's (1942, 1963) comprehensive arguments for allopatric speciation eventually resulted in widespread agreement that this mode predominates. Although there continue to appear claims of sympatric speciation, mainly in herbivorous insects and fishes, most recent such reports acknowledge that the best evidence remains circumstantial (review in Vrba 2005). It is fair to say that an expectation of predominant allopatric speciation, particularly in hominids and other large mammals, is consistent with the weight of available evidence and enjoys widespread consensus. In terms of earlier concepts of hominid phylogeny, which accepted a progression from the earliest biped to Homo sapiens with minimal branching from that lineage, one might wonder whether it is worthwhile to test causal hypotheses of hominid speciation; but recent finds indicate that “any accurate view of ourselves requires recognizing Homo sapiens as merely one more twig on a great branching bush of evolutionary experimentation” (Tattersall 1999 p 25, 2000). That is, we need to consider seriously the question of what caused lineage branching in the hominid tree.

4.2.2 Physical change as the driver of vicariance, selection, and speciation

If allopatric speciation predominates then so also must physical initiation of speciation. Vicariance is nearly always produced by tectonic and climatic change. Incipient speciation initiated by dispersal over barriers also in most cases implies the causal influence of physical change (e.g., chance Drosophila fly dispersals over the ocean always occur, whether there are islands within reach or not; it took the production of the precursor islands of the Hawaiian Archipelago for the founding of those first allopatric populations of Hawaiian drosophilids [Carson et al. 1970]). Thus, the chief causes of population size reduction and allopatry in the history of life have probably derived from physical changes. Although the relationship of punctuated equilibria to physical change was not explored in Eldredge and Gould (1972), the pattern they argued for implies independently that the initiation of speciation mostly comes about through physical change (Vrba 1980): if species are in equilibrium for most of their durations, what causal agency of the punctuation can one invoke other than physical change? The general consensus on the importance of allopatric speciation, together with the implications of punctuated equilibria and Paterson's (1978) “recognition concept” of species, led to the proposal that physical change is required for most speciation (Vrba 1980). Paterson (1978, 1982) argued that change in the fertilization system, the critical evolutionary change in sexual speciation, is most likely to occur in small, isolated populations that are under selection pressure from new environmental conditions.

4.2.3 Ecological specialists and generalists

This contrast is of general evolutionary interest (Stebbins 1950; Simpson 1953; Eldredge 1979; Vrba 1980, 1992) and is particularly germane to mammalian evolution during the climatic instability of the Late Neogene (Vrba 1987a). It has been discussed using various terminologies, such as stenotopy and eurytopy (Eldredge 1979), niche breadth (Futuyma 1979), and breadth of habitat specificity or resource use (Vrba 1987a). Specialist and generalist adaptation can be expressed in relation to different kinds of environmental variables, e.g., with respect to food intake, temperature, vegetation cover, light intensity, etc. Given the effects of the Late Neogene climatic and tectonic changes in Africa (see Sections 4.3.1 and 4.3.2 ), the distinction between species which are stenobiomic (restricted to a particular biome) and eurybiomic (ranging across biomes) is particularly relevant. As populations of a species encounter a new environment, beyond the ancestral biome range, they could in principle either diverge from their adaptation to the ancestral biome to become specialized on the new one, or become more eurybiomic by broadening their resource use to include the new biome alongside the ancestral one (Vrba 1987a, 1989a). Evolution toward eurybiomy, which is very rare (Hernández Fernández and Vrba [2005] found a large preponderance of biome specialists among living African mammals), is of special interest as it applies to Homo (Vrba 1985a, 1989a; Pickford 1991; Potts 1998; Wood and Strait 2004). Proposals that temporal and/or spatial environmental variability, namely life in fluctuating or unpredictable environments, can promote generalist adaptations have a long history of extensive discussion (Stevens [1989] reviewed the evolution of broad climatic tolerance in high-latitude environments that have a greater range of annual and longer term variation). Adaptations to strong seasonality range across life forms, from diatoms and other photosynthetic groups in polar waters (which each winter form resting spores in response to darkening, sink down dormant out of the plankton environment to germinate again when light returns [Kitchell et al. 1986]) to the deciduous habit of many plants and hibernation and long-distance migration in animals. In advanced vertebrates, complex behaviors form an important category of such adaptations, ranging from the behavioral adjustments of animals to changing temperature and aridity (Maloyi 1972) to hominine culture.

The notion of a “biome generalist species” can be subdivided as follows. The eurybiomic phenotypes can be either (A) heritable, namely genetically based and fixed, or (B) expressed as ecophenotypes, within a broad norm of reaction, in response to varying environments (Hall 2001; West-Eberhard 2003). Case (A) has two subcases. (A1) Each organism can live in more than one biome either because each organism has the needed biomic flexibility or because each organism is a specialist on resource patches which occur across biomes. An example of the latter is the aardvark, Orycteropus afer, which is stenophagous (it eats only ants and termites), a substrate specialist (it digs burrows in sandy or clay soil), and stenophotic (it is nocturnal). Yet O. afer is eurybiomic: its specialized “resource patches” range from semidesert to dense, moist woodland across Africa. (A2) There are intraspecific differences in resource use among organisms and populations, i.e., polymorphism in resource use allows the species to respond to environmental fluctuations by shifting relative abundances of the variants. An example is the African buffalo (Sinclair 1977): Syncerus caffer caffer differs in phenotype and resource use from (and lives at higher latitudes and/or altitudes with more grassland present than) the smaller, plesiomorphic phenotype S. c. nanus (in warm, forested regions). This species appears to have “rolled with the punches” of large and frequent climatic changes since the Late Pliocene mainly by changes in polymorphic frequencies. All generalist adaptations first evolve in populations, thus rendering the species polymorphic. Intraspecific adaptations and polymorphisms, which become more elaborate with repeated climatic shifting, are likely to be the most frequent responses to climatic extremes (Vrba 1992: Fig. 4c) with speciation a much rarer outcome. Living African mammals include a few species which can live across several biomes from arid, open to well-watered, mesic, and closed environments (Hernández Fernández and Vrba 2005), i.e., their habitat specificities allow very broad tolerance of environmental variation over geography and through time. Thus, the notion that each species is “specific for a particular habitat” does not equate with specificity for a particular, or single, type of environment. The term “specific” here refers to the close relationship between species and their habitats, with no connotation of environmental breadth. A species’ habitat may remain intact although it lives in strongly fluctuating environments over long time, such as the aardvark whose habitat and resources persisted as widely varying environments swept over the areas in which it lived.

4.2.4 Habitat theory and the turnover pulse hypothesis

4.2.4.1 The Turnover Pulse Hypothesis

The Turnover Pulse Hypothesis is a part of the broader “habitat theory” which focuses on species’ habitats and on the dynamic relationships between physical change, habitats, and species (Vrba 1992). It uses the predominance of allopatric speciation and the consequence that physical change is required for most speciation. Climatic changes (from global or/and local tectonic sources) result in removal of resources from parts of the species’ former geographic distributions and therefore in vicariance. Vicariance on its own is insufficient for speciation. Many species underwent repeated episodes of geographic shifting, vicariance, and reunion, of their distributions (distribution drift), in response to the astronomical climatic oscillations, without speciation although intraspecific adaptive changes may have accumulated (Vrba 1992, 2005). For speciation to occur, physical change must be strong enough to produce population isolation but not so severe as to result in extinction; and the isolated phase must be of sufficiently long duration for the changes which define speciation (adaptation of the fertilization system to the new environment; Paterson [1982]) to occur. I have suggested that most speciation requires sustained isolation, or near isolation, without rapid reintegration on the Milankovitch timescale and that shrinking populations are important in which habitat resources are dwindling, competition increases, with consequent strong selection from the changing environment (Vrba 1995b). In the absence of physical change of appropriate kind and duration, although species may accumulate new adaptations, they are buffered against speciation at several levels (review in Vrba 2005).

One prediction is that most lineage turnover, speciation and extinction, has occurred in pulses, varying from tiny to massive in scale, across disparate groups of organisms, and in predictable temporal association with changes in the physical environment (Vrba 1985b, 2005). If we think of origination, several possible patterns of origination frequency could result, all different from the temporally random pattern predicted under H 0: (1) Origination could in principle be confined to rare, large pulses in response to the largest environmental changes. Such large pulses may resemble jagged mountain crests, or dissected high plateaus, rather than simple, single peaks because the timing of turnover responses to climatic or tectonic episodes will differ among organismal groups and local areas. (2) Many, frequent, small pulses, such as in response to the 100 thousand year astronomical cycle, interspersed by the less frequent, larger ones described under (1). (3) Combinations of the random null model and the turnover pulse hypothesis suggest additional predictions such as a random background of turnover frequency punctuated by rare pulses. A comparison among turnover pulses is expected to show much heterogeneity—or “mosaic” differences. The environmental changes that trigger turnover are diverse. They vary in nature, intensity, timing—how long they endure, how much fluctuation occurs, and steepness of component changes and net trends—and in geographic emphasis and extent, from very localized to present in many parts of the earth. Topographic and latitudinal factors contribute to geographic variation in the turnover responses to a major global change. Also, the different organismal groups differ sharply in how they are affected by climatic variables (see Andrews and O' Brien 2000 for mammals). They differ in turnover response (by speciation, extinction, or by no turnover at all). Lineages which do undergo turnover initiated by a given physical change may do so with different timing (in “relays,” see examples in Vrba 1995b, c). Thus, if a turnover pulse is detected in a data set, it is desirable to study subdivisions of those data to understand the detailed taxonomic, geographic, and temporal patterns.

4.2.4.2 Additional hypotheses

(1) Under habitat theory and other concepts which invoke predominant allopatric speciation, species should generally “start small,” namely in geographic distributions that are more restricted than those they attain later on (Vrba and DeGusta 2004). H 0 does not predict this. (2) Of two areas of similar large size, both subject over the same time to climatic cyclic extremes that remain habitable for organisms, the area that is more diverse in topography will have higher incidences of selection pressures and vicariance per species. The prediction is that the topographically more diverse area has higher rates of vicariance, speciation, and extinction (Vrba 1992). (3) During periods of strong latitudinal thermal contrasts, with ice caps on one or both poles, biomes closest to the equator are predicted to have higher speciation and extinction rates than biomes at adjacent, higher latitudes (e.g., this bias may have contributed to the high species richness in the tropics today [Vrba 1985b, 1992]). (4) Biome generalists are expected to have lower rates of vicariance, speciation, and extinction than biome specialists (Vrba 1980, 1987a, 1992). Because habitat theory stresses physically initiated vicariance and selection pressure, changes in amplitude and mean of the climatic cycles, and in which cycle predominates, are expected to affect the evolutionary outcome. The larger the amplitude, the higher the incidence of vicariance and selection pressure at any cyclic extreme, accelerating the rates of intraspecific adaptation, speciation, and extinction. Changes in cyclic dominance can affect the frequency and duration of vicariance. Large translations in the climatic mean and envelope may be especially significant for speciation and extinction (Vrba 1995b: Figs. 3.2, 3.3).

4.2.5 The coordinated stasis hypothesis

Brett and Baird's (1995) hypothesis of coordinated stasis is Darwinian in its focus on organismal interactions in a community as a source of stasis. It proposes that the coevolutionary bonds during stasis are so strong that physical change is needed to disrupt them to result in turnover. Thus, this model is “community based” in its theoretical assumptions (see also the hypothesis of coevolutionary disequilibrium of Graham and Lundelius 1984; and reviews in Barnosky 2001; Vrba 2005). Brett and Baird's (1995) model predicts stasis of species, interrupted by pulses of speciation and extinction, across all communities in which a set of species occurs. Thus, their predictions are closely comparable with those of the turnover pulse hypothesis, as acknowledged by Brett and Baird (1995 p 287): “The same term [coordinated stasis] could be used for the blocks of stability in Vrba's (1985) ‘stability-pulse’ hypothesis.”

4.2.6 The variability selection hypothesis

This hypothesis was proposed and applied to hominid evolution by Potts (1998; pages quoted are from this paper). It is about (1) a particular category of adaptations which he calls “variability-selection adaptations” (VSAs), (2) their initial appearance and establishment, (3) their fate in the face of long-term climatic cycles, and (4) an interpretation of the theoretical implications of their evolution.
  1. 1.

    VSAs are “structures and behaviors responsive to complex environmental change” (p 81), which are uniform within species “yet able to mediate secondary phenotypic traits that vary …” (p 85). His examples include a locomotor system allowing a wide repertoire of movement and “a large brain or specific neurological structure that is effective in processing external data and generating complex cognitive responses” (p 85).

     
  2. 2.

    VSAs arise first in isolated populations. Intraspecific polymorphism results with VSAs in some populations and not in others. Organismal selection from short-term variability during organismal lifetimes initially promotes such VSAs (or at least allows them to persist).

     
  3. 3.

    The long-term evolutionary outcome at Milankovitch and longer timescales is that organisms with VSAs survive climatic extremes. Therefore, species which include at least one VSA-carrying population survive. Over time the VSAs can become more elaborate as climatic extremes recur. Thus, high climatic amplitude at timescales longer than organismal life times, notably at Milankovitch and longer timescales, causally influences the evolutionary outcome.

     
  4. 4.

    Climatic variability at the longer timescales is a selective agent of VSAs, which are “designed [by selection] to respond to novel and unpredictable adaptive settings” (p 85). That is, these organismal adaptations are shaped by selection for the function of flexible responses to future climatic excursions of the Milankovitch cycles; and this is a new kind of selection: “variability selection” (VS).

     

Potts claims that this hypothesis differs from all others, notably from the (p 82) “savanna hypothesis” and other “environmental hypotheses of hominid evolution [which focused] on a specific type of habitat.” He regards the VSA concept as distinct from previous concepts of adaptation, such as the generalist adaptations which confer eurytopy (Eldredge 1979), broad habitat specificity (Vrba 1987a), and broad climatic tolerance (Stevens 1989). He considers “habitat-specific” adaptations (Vrba 1987a) and selection pressures as different from VSAs and VS because the former in his view narrowly refer to a particular kind of environment and not to variable environments. I believe that he is wrong in these claims. Proposals (1), (2), and (3) are severally and jointly consistent with previous theoretical proposals (see Section 4.1.3). The sole departure is proposal (4). Structures and behaviors that confer flexibility in the face of climatic variations, and that may arise and exist as polymorphic variants in species, are well known (e.g., the resting/vegetative life cycle in diatoms noted above, hibernation, etc.) including complex behaviors in primates (e.g., the presence in some Japanese macaque populations of grass-washing behavior [Nakamishi et al. 1998]). But these adaptations require no more than selective agents during the life times of organisms. While they might fortuitously “come in handy” when the next ice age arrives, we would not claim that they must have been selected for that function. (See Williams's [1966] argument that we should not confuse selection [which “cares” only about immediate fitness of the selected] and adaptation [which is no more than the character shaped directly by selection for current function] with the incidental evolutionary effects of these phenomena; see also Gould and Vrba's [1982] distinction between adaptation and exaptation.) Also, Potts (1998) is wrong in concluding that the “habitat-specific” adaptations and selection pressures, as under habitat theory, refer narrowly to a particular kind of environment and not to variable environments. As noted earlier, “habitat” should not be conflated with “environment.” A species’ habitat may remain intact in different environments at one time and over a long time such as the aardvark whose habitat and resources persisted as strongly differing environments swept over the areas in which it lived.

The special effects which the high amplitude of the climatic cycles since the Late Pliocene had on the biota (e.g., that species, in which generalist adaptations for climatic tolerance had evolved survived disproportionately) have also been discussed (Stanley 1985; Vrba 1985a, 1992, 2000). No one doubts that strong Milankovitch excursions can selectively remove some populations and species whose organisms are unfit under those conditions or that generalist adaptations of survivors can sequentially be elaborated during recurrent such episodes. But this would not be a new kind of selection. Organismal selection cannot promote adaptations to future Milankovitch extremes, although “inter-demic selection” (Wright 1932, 1967) or species selection (review in Vrba 1989b) could in principle occur at those longer timescales. (In fact, Potts did at one stage wonder whether his notion might represent a form of lineage or species selection [R. Potts personal communications]). The problem is that the concept of selection and adaptation at levels higher than that of organisms is onerous (Williams 1966; Vrba and Gould 1986; Maynard Smith 1987; Vrba 1989b). Maynard Smith (1987) discussed this as follows (p 121): “We are asking whether there are entities other than [oganisms] with the properties of multiplication, heredity, and variation, and that therefore evolve adaptations by natural selection.” Considering the nature of the adaptations Potts (1998) had in mind, one probably does not need to invoke higher level selection. Such issues on levels of selection have been extensively debated and with respect to diverse organismal case histories. An example which is of interest here, in spite of (and perhaps because of) being far removed from hominids on the tree of life, is the case in diatoms with the resting stage adaptation to polar conditions of long winter darkness (Kitchell et al. 1986): The fossil record shows that diatoms living in Arctic waters just before the Cretaceous/Tertiary (K/T) boundary already had this life cycle adaptation. Kitchell et al. (1986) documented that during the K/T mass extinction (which involved long-term global darkening), diatoms and other photosynthetic planktonic groups with resting stages had markedly lower extinction rates than groups which lacked this seasonal adaptation. They argued (correctly in my view) that these life history features, which arose by selection at the organismal level as adaptations to seasonal variability, were also fortuitously (by sheer luck) available and useful during the K/T event for weathering much longer intervals of darkness. They concluded that this sorting among species, although nonrandom, does not represent species selection but species sorting according to the effect hypothesis (Vrba 1980). The adaptation in this case could not have been selected at the organismal level for climatic variability at the timescale of mass extinction. I suggest that the selective forces and character complexes which contributed to survival of hominids and other mammals in the face of increasing climatic amplitude during the Late Neogene may in principle fall into the same category. That is, no new kind of selection needs to be invoked.

4.2.7 Tests based on the temporal distribution of newly appearing phenotypes and species

Both the coordinated stasis and turnover pulse hypotheses predict significant concentration in time of speciation and extinction events (namely, turnover pulses). The prediction of Potts's (1998) model is that features that enhance flexibility should appear “during a period of expanding environmental fluctuation” (p 92). Most difficulties in testing such hypotheses have to do with errors in the chronological, physical, and biotic data, and with testing at inappropriate temporal, geographic, and taxonomic scales (Barnosky 2001). Vrba (2005) discussed two types of error in tests for turnover pulses: inferring pulses that are not there (i.e., erroneous rejection of H 0, type I error), and failure to detect real pulses (type II error) as exemplified by Signor and Lipps (1982). Take for an example of type II error an attempt to distinguish between H 0 and real small speciation pulses that occurred at the Milankovitch timescale. Such a test using first appearance data with lower time resolution (e.g., the data for intervals of 0.5 Myr [million years; Ma will refer to million years ago] length in Vrba and DeGusta's [2004] study of African mammals) will fail. In most available data sets, the best hope lies in testing whether or not large turnover pulses can be detected. The main bias that leads to type I error, seeing pulses that are not there, arises from unequal fossil preservation between time intervals, areas, and groups of organisms, the “gap bias” (Vrba 2005): any given species’ fossil FAD (first appearance datum) may postdate its true, or cladistic, FAD (Kimbel 1995). Gaps have the effect that, for instance, a count of FADs in an interval is erroneously inflated by species’ records that in reality originated (but were not detected) previously. An early version of a test that corrects for the “gap bias,” thus allowing a rigorous test of the pulse hypothesis, was applied to the African larger mammals of the past 20 Myr divided into 1-Myr- long intervals (Vrba 2000). More recently, a second updated form was applied to the nearly 500 species recorded over the past 10 Myr divided into 0.5-Myr long intervals (Vrba and DeGusta 2004; Vrba 2005). Time resolution in this record is sufficiently good, with more than 70% of the site records dated by radiometric or paleomagnetic means, that any large speciation (or extinction) pulses spaced 1 Myr apart should be detectable. Some results will be mentioned in Section 4.3.3 .

4.3 Physical change, adaptation, speciation: evidence from the African Neogene

4.3.1 Physical background: climatic change

Following the definitive documentation of the astronomical cycles (Hays et al. 1976), it was thought that they may have had little effect on the tropics in general (review in Burckle 1995) and on African hominid-associated environments in particular. For example, Hill (1995 p 187) considered that: “it may be that African terrestrial vertebrate habitats were to some extent buffered from climatic changes seen elsewhere.” Hill's caution is well taken that specific areas may “march to a local drummer” especially if that drumbeat derives from tectogenesis (see below). It now appears that much of Africa participated in the global changes. The Late Miocene-Recent record is relevant as the earliest hominid fossils currently date to ca.7 Ma (Brunet et al. 2004).

4.3.1.1 The Late Miocene

There was ice buildup on West Antarctica and general increase in δ18O values 7–5 Ma (Miller and Fairbanks 1985; Kennett 1995). A major cooling which started before 6 Ma and peaked shortly thereafter contributed to isolation and desiccation of the Mediterranean Basin during the Messinian low-sea-level event and salinity crisis dated ca. 5.8–5.3 Ma (Haq et al. 1980; Hodell et al. 1994; Bernor and Lipscomb 1995; Aifa et al. 2003; Garcia et al. 2004). This was followed by warming and a post-Messinian transgressive phase starting before 5 Ma to reach a maximum in the 5- to 4-Myr interval (Haq et al. 1987). Reviews of the numerous and often major changes—both physical and biotic—on the continents and in the oceans, and particularly in Africa, can be found in Brain (1981) and Vrba et al. (1995). Questions remain on the African effects of these Late Miocene climatic events. Kingston et al. (1994) found that, in the Kenyan Tugen Hills area, a heterogeneous environment with a mix of C3 and C4 plants—and without grassland dominance—persisted over the entire past 15 Myr without any apparent local influence from global climatic change. Evidence from Lothagam indicates that this part of Kenya experienced strong environmental changes over the latest Miocene (Leakey et al. 1996; Leakey and Harris 2003). Further evidence comes from analyses of carbon isotope ratios in soils and fossil tooth enamel. Cerling et al. (1997) studied fossil herbivores ranging over the past 22 Myr from several continents. Using the fact that low δ13C values in herbivore teeth reflect a diet of mainly C3 plants while high values indicate feeding on C4 plants, they found that up to 8 Ma, mammals in Pakistan, Africa, and South and North America had C3 diets or C3-dominated diets. By the late to latest Miocene C4-plants came to dominate the diets. In Kenya, representing the lowest latitude in the sample, the transition was complete by between 8 and 6.5 Ma, and in Pakistan by ca. 5 Ma. Cerling et al. (1997) interpreted their results as showing a global increase in the biomass of C4 plants between 8–6 Ma which resulted from a decrease in atmospheric CO2.

4.3.1.2 The Plio-Pleistocene

Much evidence by now suggests that many parts of Africa during the Plio-Pleistocene were indeed responding to orbital variations and certainly to the strongest global events (reviews in Vrba et al. 1995; Reed 1997; Potts 1998; deMenocal 2004). Continuous Plio-Pleistocene records which demonstrate this are now known from western, eastern, northern, and southern Africa: Pollen cores off West Africa record the shifting of the Sahara–Sahel boundary and the earliest extensive spread of the Sahara desert ca. 2.8–2.7 Ma (Dupont and Leroy 1995). Marine records off West Africa and from the Gulf of Aden document δ18O variations, and also dust influxes from the Sahara and Sahel regions in the West, and from Arabian and northeastern African areas in the Gulf of Aden (DeMenocal and Bloemendal 1995; deMenocal 2004). A record of aeolian grain size from the Gulf of Aden shows changes in the intensity and phase of the Indian monsoon (Clemens et al. 1996). A northeastern African record shows that sapropels (organic-rich black layers) were deposited during humid periods in the eastern Mediterranean Sea following high-flood periods of the Nile River at the tempo of orbital precession (Rossignol-Strick et al. 1998). For southwestern Africa, a record of the past 5 Myr off Namibia, underlying the Benguela upwelling system, yielded a continuous time series of changing sea surface temperature (SST) for the past 4.5 Myr, with decreased upwelling interpreted to represent warmer conditions with wetter, more mesic periods in southern Africa (Marlow et al. 2000). A marine record off Angola derived from compound-specific carbon isotope analyses of wind-transported terrigenous plant waxes, indicated African C4 plant abundances during the interval 1.2–0.45 Ma and showed that the African vegetation changes are linked to SST in the tropical Atlantic Ocean and that changes in atmospheric moisture content due to tropical SST changes and the strength of the African monsoon controlled African aridity and vegetation changes (Schefuss et al. 2003). The phase relationships between the African monsoon and the glacial cycles were shifting continuously (Clemens et al. 1996), explaining why indicators of surface water, such as lake levels, and of vegetation, such as dust spikes, do not always covary (deMenocal et al. 1993).

The major events and steplike changes identified by these and other authors are as follows. There were significant shifts in the intensity and phase of the Indian monsoon at ca. 2.6, 1.7, 1.2, and 0.6 Ma (Clemens et al. 1996). Marlow et al. (2000) concluded that SSTs decreased markedly, in association with intensified Benguela upwelling, after 3.2 Ma, with subsequent periods of marked SST decrease and upwelling intensification near 2.0 and 0.6 Ma. DeMenocal and Bloemendal (1995) documented a shift from dominant climatic influence occurring at 23–19 thousand year periodicity prior to ca. 2.8 Ma to one at 41 thousand year variance thereafter, with further increases in 100 thousand year variance after 0.9 Ma (see also Ruddiman and Raymo 1988). DeMenocal (2004) summarized his conclusions on consistent patterns of African subtropical climatic variability, based on the West and East African records analyzed by him and others, as follows (p 8): “1. Orbital-scale climatic variability persisted throughout the entire [Plio-Pleistocene] interval extending in some cases into the Miocene…. 2. The onset of large-amplitude African aridity cycles was closely linked to the onset and amplification of high-latitude glacial cycles. 3. Eolian concentration and supply (flux) increased gradually after 2.8 Ma. 4. Step-like shifts in the amplitude and period of eolian variability occurred at 2.8 (±0.2) Ma, 1.7 (±0.1) Ma, and 1.0 (±0.2) Ma. 5. Evidence for 104–105 year ‘packets’ of high- and low-amplitude palaeoclimatic variability which were paced by orbital eccentricity.” Using records of δ18O variation since the Late Oligocene, Potts (1998) subtracted the lowest from highest value for each unit million year as a measure of total climatic variability. He found that variation of 0.3–0.5 parts per mil (ppm) was obtained for most of the Neogene until the 6.0- to 5.0-Myr interval, during which variability rose sharply. After a minor decrease during 5–4 Ma, there were increases during every succeeding interval with the highest one to 1.9 ppm, during the past 1 Myr (Potts 1998 p 83: Fig. 1).

I used Shackleton's (1995: Fig. 17.3) data, which records δ18O variation at 0.003-Ma interval steps for the past 6 Myr, to identify periods over which the largest net cooling or warming trends occurred. (Vrba 2004: take an interval t x of length x thousand year, for example t 100 for x = 100 thousand year, and move it step by step along the time axis from early to late. At each interval step, mark the interval along the time axis if either of conditions C, for cooling, or W, for warming, is true: C: the upper [warm] envelope of the climatic curve remained continuously below the running mean of the previous 300 thousand year; i.e., the interval is a t 100,C , or an interval of length 100 thousand year with marked cooling. W is the corresponding condition for a warming trend. A pattern of t 100,C and t 100,W distribution in time results, with data clusters for the most sustained trends. I here report results for separate assessments using interval lengths in x thousand of year of x = 40, 65, 100, 140.) The following approximate intervals (in chronological sequence) emerged as times of sustained net cooling (t 40,C, t 65,C, t 100,C, t 140,C, are respectively labeled *, **, ***, ****, from least to most severe; time ranges in ca. Ma): 5.1–4.90*, 4.1–3.95*, 3.45–3.25***, 2.7–2.35**** (and 2.9–2.5*), 2.1–2.0*, 1.8–1.65**, 0.95–0.85**, 0.8–0.65** (and 0.8–0.6*). Intervals of net warming (similar notation as for cooling): 5.6–5.35****, 4.5–4.4*, 3.1–2.9*, 1.65–1.6*, and ca. 0.85*. Hypotheses under habitat theory predict that such strong longer-term climatic trends should be associated with higher frequencies of evolution in general and of speciation and extinction particularly. (The predictions of the variability selection hypothesis [Potts 1998] do not differ substantively from this: times of strong change in climatic mean are also those of increased variability as measured by Potts [1998]. For times of increased variability without strong change in climatic mean, both predict an increase in intraspecific adaptation including adaptation which confers increased flexibility in the face of the climatic extremes.)

The precise relationships between the different kinds of evidence cited are incompletely understood; and, as expected, time estimates for significant climatic events do not neatly coincide. We are far short of having a set of “paleoclimatic magic numbers” (Lewin 1984 p 154) for comparison with hominid evolution. Nevertheless, it is worth noting the rough consensus on periods of major change: during the latest Miocene these included that toward 6.5 Ma and that associated with the Messinian ca. 5.8–5.3 Ma; but the African effects of changes over this general time period are less well defined because of a paucity of long records. Several intervals during the Plio-Pleistocene stand out (in approximate descending order of magnitude in ca. million years): notably 2.9–2.3, 3.5–3.2, 1.8–1.6, 1.2 and 1.0–0.6, and possibly also ca. 5 Ma, toward 4 Ma, and ca. 2 Ma.

In sum, hominid and other lineages faced net increase in seasonal cooling, aridification, and vegetational opening (see Brain [1985] on how cooler winters promote reduced height and wider spacing of tree cover in Africa). These variables have strong effects on species distribution and richness today (e.g., Andrews and O' Brien [2000] found that plant species richness and thermal seasonality were the most important such factors in modern southern African mammals as a whole and in large mammals annual temperature as well). Resource availability was fluctuating at seasonal to Milankovitch timescales and at intermediate (Potts 1998) and longer timescales. While over the long term cooling and aridification were both increasing and many African records show that association, it is by no means invariable as expected from the shifting phase relationship between the monsoon and glacial cycles. For example, pollen data from Hadar, Ethiopia, shows that “Australopithecus afarensis accommodated to substantial environmental variability between 3.4 and 2.9 Ma ago. A large biome shift, up to 5°C cooling, and a 200- to 300-mm/year rainfall increase occurred just before 3.3 Ma, which is consistent with a global marine δ18O isotopic shift” (Bonnefille et al. 2004 p 12125).

4.3.2 Physical background: tectonism

Tectogenesis has featured less prominently than climate change in discussions of evolution, perhaps because it is mostly a slow process and date limits for events tend to be wide. Yet it has had a primary influence on landscape and biotic evolution. This includes hominid evolution especially in rift-associated environments as recognized long ago by Coppens (1988–1989). Crustal changes influenced climate on a grand scale, e.g., Late Pliocene closure of the isthmus of Panama may have led to the start of the modern ice age (Maier-Reimer et al. 1990; Haug et al. 2001). Uplift of western North America, the Himalayas, and the Tibetan Plateau, possibly influenced the Pleistocene cooling intensification at ca. 1 Ma (Ruddiman et al. 1986). Northward drift of Africa during the Neogene led to southward displacement and areal decrease of tropical African forests and contributed to long-term aridification (Brown 1995). Episodes of intensified African uplift since ca. 30 Ma, which raised the entire eastern surface higher than in the West, greatly affected the African climate (Burke 1996). Apart from the numerous localized climatic effects of tectogenesis (Feibel 1997), the topographic diversity it generates together with the superimposed climatic cycles constitutes a prime cause of spatial and temporal environmental heterogeneity, changing selection pressures and speciation (Vrba 1992). Thus, evolution of the African Rift had an especial role in some evolutionary events in hominids (Coppens 1988–1989) and other mammals (Denys et al. 1987). The present episode of rifting began in the Early Miocene (Frostick et al. 1986). Between Ca. 8 and 6 Ma, a general increase in African tectonic activity led to formation of the Western Rift (Ebinger 1989). A major episode of uplift coincided with the climatic changes ca. 2.5 Ma (Partridge and Maud 1987). After 6 Ma, the rift system continued to propagate to the southwest toward the Kalahari Craton (Summerfield 1996). One incipient zone of rifting, trending southwest from Lake Tanganyika, terminates in central Botswana, where faulting and tilting of the zonal margins have resulted in damming of the Okavango River to spread out as the extensive inland Okavango Delta (Scholz et al. 1976).

I suggest that the dynamics of the hydrological features associated with rifting – rivers redirected, lakes forming and disappearing, and especially the inland deltas spreading at the margins of incipient rift zones – have had a particular impact on the evolution of hominids and other biota. All early hominids required permanent water, and many of the eastern African hominid sequences reflect riverine and rift-margin associated deltaic and lake environments (Harris et al. 1988; Brown and Feibel 1991). The significance of inland deltas is that they can form vicariated “islands” of mesic conditions—or refugia—throughout periods of aridification and even in the absence of topographic heterogeneity. The edges of such a refugium are ecologically heterogeneous with intrusions of the arid surrounding environment. (“Refugium” here means a biome refugium, e.g., a forest refugium preserves the characteristic forest vegetation physiognomy, although its detailed taxonomic composition may differ from that of the parent forest community.) The Okavango Delta provides a good example: it is a vicariant island—despite the very low relief of the area (Scholz et al. 1976)—of woodland savanna and water almost entirely surrounded by semidesert. Vrba (1988) suggested that many of the hominid-bearing strata represent times when the areas were such inland deltaic-riverine-lacustrine refugia and that this poses problems for our ability to recognize times of widespread climatic change across the larger areas because “climatic change in the larger region is recorded in a refugium only close to its ecotonal limits, by the new appearances (or disappearances) of peripheral taxa … that represent occasional intrusive elements from the alternative biome” (p 410). An important implication from the evolutionary perspective is this: as climatic changes were sweeping across much of Africa at the Milankovitch scale, so such inland deltas were recurrently isolated and reconnected as parts of larger continuous biomes. During the reconnected phases, migration and gene flow occurred. During the vicariant phases there was enhanced incidence of gene pool divergence among populations, selection pressures at the refugial margins, intraspecific phenotypic diversification, and speciation. If true that inland deltas can in this way act as centers of phenotypic diversity and speciation and that they are particularly prevalent at the tilting margins of incipient rift zones, this would predict a Late Neogene propagation of centers of increased speciation in a south-southwesterly direction as the rift evolved.

4.3.3 The record of first appearances of mammalian species

4.3.3.1 All larger mammals

As noted above, a method which corrects for the “gap bias” was applied to the African larger mammal record of the past 10 Myr. Such correction is especially important in the Late Neogene climatic context because open, mesic to arid areas tend to preserve vertebrate fossils better than do the more forested, wetter ones (Hare 1980). The following results emerged (largely agreeing with those in Vrba [1995c, 2000], in so far as they are comparable): Over the past 8 Myr, the strongest turnover pulses, involving both origination and extinction, occurred in the 5.5- to 5.0- and 3.0- to 2.5-Ma intervals. (The division into equal time intervals is artificial. The dating of the earlier pulse is tentative and this event may be closer to 5.5 Ma, or just before, than to 5 Ma; I will refer to the 5.5-Ma event. The Late Pliocene changes are better delimited between ca. 2.8 and 2.3 Ma.) Each of the intervals 7.0–6.5 and 3.5–3.0 Ma had an origination pulse without an extinction pulse and 1.0–0.5 Ma an extinction pulse without an origination pulse. Where one can compare this set of turnover events with the strongest cooling trends, the coincidence in time and intensity is strikingly close: the strongest climatic event, cooling toward ∼2.5 Ma, coincides with the strongest turnover pulse, while lesser cooling and turnover events are present in the intervals 3.5–3.0 and 1.0–0.5 Ma. The results also showed intervals of significantly low origination and extinction, some of which overlapped with periods of high sea level with low polar ice on a warmer earth (Haq et al. 1987; Hodell and Warnke 1991).

The African mammalian record, and the bias-correction model which was used, continue to be updated. The results do give preliminary support to the hypothesis that at least a substantial part of turnover in African mammals was initiated by climatic change and that global cooling with increased aridity and seasonality was a more important stimulus of turnover than was global warming (Vrba 2000, 2005). Of the cooling trends, the one toward 2.5 Ma was the strongest, followed by a lesser trend starting ∼1 Ma. Yet individual glacial maxima became colder after 2.5 Ma, especially after 1 Ma (Shackleton 1995). The fact that there were no further major origination pulses after 2.5 Ma suggests that most of the lineages present then were either species that had evolved during the start of the modern ice age with adaptations to the new environments or long-lasting biome generalists that survived right through that cooling trend.

A related result is that of Vrba and DeGusta (2004). We studied the question whether most species “start small,” namely in geographic distributions that are more restricted than those they attain later on. We used the same 10-Myr long record of the African larger mammals and the correction for the “gap bias.” The number of fossil site records, from which each species is known in an interval, was taken as a proxy for the magnitude of its living geographic range and abundance in that interval. We then tested H 0 that the geographic spread of species remained averagely constant across successive survivorship categories, namely from the first appearance (FAD) interval to the immediately following one, and so on. We found that the mean number of site records increased strongly from the FAD interval to the following survivorship interval, followed by a less marked although still significant increase to the next interval, with no significant changes thereafter. Thus, we concluded that the average large African mammal species has indeed started its life in a relatively small population, and thereafter increased in geographic range to reach its long-term equilibrium abundance by ca. 1 Ma after origin. This supports hypotheses of speciation that accord a major role to the formation of isolated populations of reduced size initiated by physical change.

Not everyone has agreed that global change was a driver of evolutionary change and speciation in African hominids and other mammals. Kingston et al.'s (1994) conclusion for the Tugen Hills area in Kenya that similar heterogeneous environments persisted over the past 15 Myr without any apparent local influence from major global climatic episodes is not necessarily at variance with my findings for all larger African mammals. It seems possible that the effects of tectonism in the Tugen Hills locally dominated any signal in the area from widespread climatic change. One aim of Behrensmeyer et al. (1997) was to test Vrba's (1995c) finding of a turnover pulse in African mammals between ca. 2.8 and 2.5 Ma by examining the past 4.5 Myr in the Turkana Basin (including the northern Shungura Formation, Ethiopia, and the southwestern Nachukui and southeastern Koobi Fora Formations in Kenya). They concluded that there was “no major turnover event between 3.0 and 2.5 Myr” (p 1591) and that this “weakens the case for rapid climatic forcing of continent-scale … faunal turnover” (p 1593). I have reservations about their methods and assumptions which differed substantially from mine (Vrba 2005). A reexamination of Turkana Basin evolution over 4–1 Myr divided into 0.5-Ma long intervals, using my African mammal data base and the statistical “gap bias” model outlined above, showed a single significant origination pulse in the 3.0- to 2.5-Ma interval and no extinction pulses (Vrba 2005). Separate examination of the northern and two southern areas of the Turkana Basin indicated a strong speciation (and extinction) pulse in the North 3.0–2.5 Ma, but none in the combined or separate southern areas. This result is consistent with the southward spread of the Sahara Desert in the latest Pliocene (Dupont and Leroy 1995), which affected the northern basin more strongly, eliciting significant turnover, while the southern deltaic-lacustrine areas may have behaved more nearly like biome refugia.

At least some studies show that the larger mammalian turnover pattern is also reflected in small mammals. Among micromammals of the Shungura Formation, Ethiopia (Wesselman 1995), at 2.9 Ma, woodland taxa predominated and even rainforest taxa were present (e.g., the bushbaby Galago demidovii, a rainforest species today). These forms were displaced by new grassland-to-semidesert species by 2.4 Ma. The turnover includes terminal extinctions, immigrants from Eurasia, such as a hare, Lepus, and global first appearances of species such as a new species of Heterocephalus, the genus of desert-adapted naked molerats, and a new species of the ground squirrel genus Xerus (Wesselman 1995). This time also marks the first African and global debuts in the record of several species of bipedal, steppe-, and desert-adapted rodents such as the genus Jaculus of desert gerboas (Wesselman 1995) and a new springhare species, Pedetes, in South Africa.

4.3.3.2 The hominid record

The hominid sample is too small (15 to more than 20 species depending on which sources are consulted) to test whether most hominid species “started small” and to test for turnover pulses using the statistical methods which were applied to all larger mammals. Nevertheless, it is of interest to compare the known hominid FAD record with the timing of major climatic trends and speciation pulses in all larger African mammals. The earliest appearance of hominids, Sahelanthropus from Chad (Brunet et al. 2004; ca. 7 Ma; the hominid clade originated 8–5 Ma based on molecular estimates, Ruvolo 1997), forms a part of the elevated mammalian origination during 7–6.5 Ma and falls in an interval marked by increased African tectonic activity (Ebinger 1989) and ice buildup in West Antarctica with global cooling (Kennett 1995). Ardipithecus is first recorded just before 5.5 Ma (Haile-Selassie 2001), close to the turnover event in mammals and the major cooling and regression events associated with the Messinian ca. 5.8–5.3 Ma. One may question whether climatic change was a factor in the origin of A. ramidus because the Aramis stratum in which it occurs seems to represent a wooded and perhaps forested environment (WoldeGabriel et al. 1994). But as argued below in Section 4.3.4 , this may not preclude the initiation by physical change of speciation in this case.

Most African FADs of hominid species are Pliocene to mid-Pleistocene in age during which the intervals of strongest climatic change were (in roughly descending order of magnitude, in ca. Ma; see Section 4.3.1.2 ): 2.9–2.3, 3.5–3.2, 1.8–1.6, 1.2 and 1.0–0.6, and possibly also ca. 5 Myr, toward 4 Ma, and ca. 2 Ma. Together these cooling episodes occupy ca. 40% of the past 5 Ma. Yet most, and possibly all, of the hominid FADs either coincide with or fall very close to one of these cooling events (chronology after Wood and Richmond 2000): Australopithecus anamensis and A. afarensis, FADs ca. 4.2 Ma; FADs of A. bahrelghazali, Kenyanthropus platyops, and possibly also A. africanus are a part of the origination pulse in the 3.5- to 3.0-Ma interval; Australopithecus garhi, Paranthropus aethiopicus, P. boisei, and possibly also Homo habilis and H. rudolfensis have FADs in the 2.8- to 2.3-Ma interval. FADs of H. ergaster, H. rudolfensis, and of H. erectus (and its migration to Eurasia) fall between 2.0 and 1.8 Ma. While taphonomic factors and chance may have contributed to this pattern, it does leave intact the hypothesis of climatic cause of hominid speciation. An important splitting event in the hominid clade was the one that led to Paranthropus on the one hand and Homo on the other. Several systematic studies have concluded that the characters of A. afarensis are consistent with it being the common ancestor of Paranthropus and Homo and possibly also of one or more additional lineages (Kimbel 1995; Asfaw et al. 1999). After enduring in apparent equilibrium since at least 4.2 Ma, A. afarensis is last recorded just after 3.0 Ma (Kimbel et al. 1994), while its descendants appear variously between 2.7 and 2.3 Ma. Kimbel (1995 p 435) concluded: “regardless of which phylogenetic hypothesis is more accurate, it is clear that a pulse of speciation occurred in the hominid lineage between 3.0 and ca. 2.7 Ma, producing at least three lineages.” The phylogenetic pattern, of an inferred ancestor ending near 2.9, with new descendants branching off between 2.9 and 2.3 Ma, is common in bovids (Vrba 1995c, 1998a). These concordant genealogical patterns among different mammalian groups strongly suggest the causal influence of the start of the modern ice age, namely that common causal rules connect the climate system with evolution of different biotic groups. It remains to be seen whether additional information in future will support these preliminary indications that major climatic cooling trends and the concomitant changes in African environments were important causal influences on speciation in Hominidae, just as they were in many other mammalian lineages.

4.3.4 Climate and adaptation

There is widespread agreement that many of the Late Neogene mammalian morphological and behavioral changes, including in hominids, are overall broadly consistent with the extraordinary climatic fluctuations, and net cooling and aridification, over that time. But the precise nature of the environmental stimuli and of the processes they set in motion remain elusive. Nowhere is this more true than in the case of the origin of human bipedalism. According to Harcourt-Smith and Aiello (2004), the earliest evidence for bipedalism is arguably from Sahelanthropus tchadensis dating to 7–6 Ma (Brunet et al. 2002), Orrorin tugenensis ca. 6 Ma (Senut et al. 2001), and Ardipithecus ramidus kadabba first recorded just before 5.5 Ma (Haile-Selassie 2001). Wood and Richmond (2000) considered the tibia of Australopithecus anamensis (ca. 4.2 Ma; Leakey et al. 1995), the earliest undisputed evidence of bipedalism. Morphological evidence of a commitment to long-range bipedalism (e.g., long legs, large femoral head) appeared much later, ca. 1.6 Ma, in the postcranial skeleton KNM-WT 15000 from Nariokotome, West Turkana (Brown et al. [1985], who assigned it to H. erectus; Wood and Richmond [2000], included it in H. ergaster). The onset of this morphology in the fossil record falls into one of the periods of strong climatic change toward seasonal aridification and a greater prevalence of open vegetation. The ecological and evolutionary implications of the bipedal record before this time remain a matter of unresolved debate. Harcourt and Aiello (2004) reviewed the evidence (including the Laetoli footprints, the AL 288-1 A. afarensis skeleton, postcranial material from Koobi Fora, the Nariokotome H. ergaster skeleton, “Little Foot” [Stw 573] from Sterkfontein, South Africa, fossils of Orrorin, Ardipithecus, and Sahelanthropus) and proposed a greater diversity in bipedalism in earlier hominids than previously suspected. Such independent evolution of different styles of bipedalism within the hominid clade by itself suggests that environmental change was a cause. In each of their three phylogenetic scenarios (Harcourt-Smith and Aiello 2004: Fig. 4), the postcranial diversification coincides broadly with the 3.0- to 2.3-Ma period of the largest Pliocene climatic trend. Stanley (1992) accepted that species of Homo were the first hominids to show adaptations to open arid environments and argued that climatic change was the cause. He hypothesized that the earlier gracile australopiths did not have expanded brain sizes due to their semiarboreal mode of life which necessitated that neonates be mature enough to cling to climbing mothers. The onset of an increased encephalization quotient (EQ: based on brain volume corrected for body weight) required that neonates be born in a more altricial state and unable to cling to mothers. Thus, only once semiarboreality was abandoned could encephalization evolve.

It had long been accepted that Late Miocene African environmental change, from widespread forest to more open vegetation, resulted in new selection pressures and thus set the stage for the origin of bipedalism (the “savanna hypothesis”). Specific hypotheses of what caused the adoption of upright posture in such a context have included (reviews in McHenry 1982; Preuschoft 2004): carrying, display or warning, new feeding adaptations, control of body temperature, tools, stone throwing, and wading in shallow water. McHenry (1982) thought that hominid bipedalism “could have arisen as an energetically efficient mode of terrestrial locomotion for a small-bodied hominoid moving between arboreal feeding sites”(p 163). Recent paleoecological findings for the earliest hominids have led to doubts of the savanna hypothesis. For example, Pickford et al. (2004) found a water chevrotain Hyemoschus aquaticus, indicating dense rainforest, in the Mabaget Formation, Kenya, dated 5.3–4.5 Ma, and associated with a hominid species. The evidence associated with Ardipithecus at Aramis in Ethiopia indicates a relatively closed, tree-dominated habitat (WoldeGabriel et al. 1994). Clarke and Tobias (1995) proposed that the foot bones from Sterkfontein Member 2 (Stw 573, Little Foot, dated ca. 3.5–3 Ma) reflect a foot that had not sacrificed arboreal competence or hallucial opposability and that this suggests dense tree cover in the environment. Based on fossil pollen, it has been suggested that the preferred habitat of A. africanus at Makapansgat was subtropical forest and that selective pressures associated with densely vegetated environments played a role in the evolution of bipedalism (Cadman and Rayner 1989; Rayner et al. 1993). Potts (1998) dubbed this the “forest hypothesis” of bipedal origin and countered it by pointing out that most of the Late Miocene–Pliocene hominid species appear to have lived in varied habitats ranging from closed to more open conditions. The fossil bovids associated with A. africanus at Makapansgat and Sterkfontain do not suggest a uniform forest, although a mosaic in the greater area which includes densely wooded patches could be consistent (Vrba 1974, 1980, 1987b), which agrees with Reed's (1997) conclusions.

I believe that our inferences of evolutionary process from paleoenvironmental reconstruction have been too crude and rigid. Consider three points in relation to the focus on the forest-to-savanna spectrum in the debate on hominid origin: (1) If a species, such as Ardipithecus ramidus, is found associated with “forest” and its inferred ancestor also lived in “forest,” there may have been differences in the nature of the forest which were not recorded in available evidence, but which had bearing on the evolution of the descendant species. (2) Even if the vegetation was identical, the descendant species may still have speciated by vicariance due to climatic or other physical change. Among living African mammals, there are many pairs of rainforest-adapted sister-species which speciated from forest-adapted ancestry following climatic vicariance (Grubb 1978). That is, the fact that the ancestral and descendant species both live(d) in forest does not mean that climatic change did not bring about speciation. (3) Even if the ancestral and descendant vegetational environments were identical, physical change may have altered other environmental aspects that brought new selection pressures and precipitated speciation. Patchiness does not only derive from vegetational heterogeneity. It can result from diverse factors including intrusive wetlands and other hydrological features, topographic barriers introduced by tectogenesis (such as rocky barriers), and lava or ash flows (e.g., Gulick [1872] showed that lava flows had very probably initiated speciation in the Hawaiian snail fauna). Selection pressure for traversing the barriers to reach the other side (which may have been what the A. afarensis individuals who formed the Laetoli footprints were doing; Leakey and Hay 1979) or for foraging in these areas (as in a shallow delta or wetland) might have been relevant to selection for onset or, later on, elaboration of bipedality. The notion that wading in shallow water played a part (Niemitz 2000; Verhaegen et al. 2002) seems reasonable given what we know about the paleoenvironments of many early hominid species.

There is some agreement that the onset of advanced bipedalism in Homo close to ca. 1.6 Ma not only falls during a time of change to more open and seasonally arid landscapes but also makes sense as a selective response to these changes. Potts (1998) pointed out that by the latest Pliocene, populations of Homo were increasingly mobile, for example, tool-making behavior involved long-distance transport of stones as far as 10 km. Increased mobility is reflected by the migration out of Africa by 1.8 Ma of a lineage of Homo (if the early date for H. erectus in Java, Indonesia, is correct [Swisher et al. 1994]), the first of many subsequent migrations out of Africa which were associated with physical changes (Stringer 1995; Tattersall 1997b; Klein and Edgar 2002).

Other hominid phenotypes also appear at times of—and are adaptively consistent with—similar climatic changes. Stone tools appear by 2.6–2.5 Ma near the end of the large Late Pliocene cooling trend (de Heinzelin et al. 1999; Semaw et al. 1997). Hatley and Kappelman (1980) proposed that the climatic change led to this behavioral advance. They showed that a high below-ground plant biomass is characteristic of xeric open areas and argued that digging out of such foods, first by hand and later by digging sticks and other tools, evolved as an important feeding strategy of early hominids when the African savanna became more open and arid. From Bouri in Ethiopia comes the earliest evidence of tool use to butcher large mammal carcasses dated 2.5 Ma (de Heinzelin et al. 1999). The onset of more expanded tool kits appears to overlap with the climatic events ca. 1.8–1.6 Ma (Leakey 1971). Other behavioral changes may also date to the Plio-Pleistocene transition. For instance, the fact that the mandible and postcanine tooth crowns of H. ergaster (dated ca. 1.9–1.5 Ma), when scaled to body mass, are no larger than those of modern humans, may reflect earliest cooking (Wood and Richmond 2000). According to Wood (1995), the first signs of the “hypermasticatory trend” occurred with advent of Paranthropus aethiopicus ca. 2.6 Ma, followed by exaggeration in this trend ca. 2.3 Ma with the FAD of P. boisei, and further lesser modifications to the dentition of this species between 1.9 and 1.7 Ma.

The Late Pliocene and Pleistocene behavioral and cultural advances reflect reorganization and expansion of the brain. Although the available evidence indicates significant EQ increase in Homo only over the past 2 Myr (Holloway 1970, 1972, 1978; McHenry 1982), Holloway et al. (2003) presented evidence that brain reorganization predated brain expansion in hominid evolution. I previously suggested that the encephalization trend in Homo “evolved by progressive prolongation of ancestral, fast, early brain growth phases. It started with the modern ice age and was fuelled by progressive intensification of cooling minima since then” (Vrba 1996 p 15). I still suspect that we may find future indications that some of the brain modifications which came to characterize Homo—perhaps not increase in EQ but brain reorganization—were promoted by the start of the modern ice age. The largest EQ increase occurred between ca. 600–150 thousand year ago (opera cit.), toward the end of the mid-Pleistocene strong climatic events of ca. 1.0–0.6 Ma. Many selective scenarios for encephalization in Homo have been proposed. Falk's (1980) review included warfare, language, tools and labor, hunting, and heat stress. Gabow (1977) emphasized population structure and culture, McHenry (1982) language, and Brain (2001) our predatory past. Vrba (1985a, 1988, 1989a) proposed that major selection pressures that led to brain and cultural evolution derived from the large-scale changes in climatic mean and amplitude during the Plio-Pleistocene; and that culture and the underlying brain modifications in Homo represent adaptation to eurybiomy or “generalist adaptation. Hominine culture is an extension of the common phenomenon in other animals that use behaviour to cope with climatic conditions. … a special case among animal behaviours that confers an expanded use of environmental resources” (Vrba 1989a p 30). As cited above, Potts (1998) made a similar proposal to explain the brain and behavioral adaptations of Homo. Others have also argued that Homo evolved toward biome generalization (Wood and Strait 2004).

The notion that robust australopiths, Paranthropus, were in certain senses specialists was originally proposed by Robinson (1963) based on the dentition of P. robustus. He suggested that the “crushing, grinding” robust vegetarian specialist lived in a somewhat wetter and more luxuriant environment than did the earlier gracile omnivore A. africanus. I suggested that the musculature of P. robustus was massive and the molars proportionally large “because their ‘vegetables’ were of the tough grassland type” (Vrba 1975 p 302) and that, in contrast to the more generalized Homo, “robust australopithecines were more specialized on open arid habitats” (Vrba 1989a p 30). The first really thorough analysis of the proposal that Paranthropus species were feeding specialists is that by Wood and Strait (2004). They concluded that Paranthropus species were most likely ecological generalists (i.e., eurybiomic in being able to make a living in varied environments) and made the novel proposal that (p 149) “… although the masticatory features of Paranthropus are most likely adaptations for consuming hard or gritty foods, they had the effect of broadening, not narrowing, the range of food items consumed.” I accept their arguments which accord well with available ecological information for Paranthropus. The acquisition, in response to newly encountered environments, of morphology which can perform a new specialized function, but which at the same time permits the retention of functions evolved in the ancestral more uniform environment, is a recurrent theme in the evolution of generalists. An example from other mammals occurs in the impala Aepyceros melampus which based on its cladistic placement (Vrba and Schaller 2000) evolved from a browsing ancestry. During the Plio-Pleistocene, this lineage evolved cranial and dental features which allow mastication of grass and other tough plant matter. The impala also has a stomach structure which undergoes reversible seasonal changes (Hofmann 1973), a rare adaptation to varied vegetational environments. As a consequence of these dental and digestive evolutionary advances, the impala is today a consummate herbivore generalist which can subsist in different environments by switching its dietary intake.

A comparison of the hominid evolutionary changes with those in other mammals is beyond the present scope. But it is worth noting that there are numerous examples of anatomical and behavioral changes in mammals, which not only appear during roughly the same time periods when hominid novelties appeared but which also show similarities in the nature of the changes and in their ecological effects. Turner and Wood (1993) studied the times of appearance in the record of dental changes in various African mammals. They concluded that dental modifications for herbivory in more seasonally cold and arid conditions did show consistent temporal patterns among themselves and with those of some hominids (p 301): “changes in dental morphometrics support the interpretation of the development of savanna environments in response to colder and more arid conditions across the larger mammal fauna of eastern and southern Africa. The hypermasticatory development of Paranthropus was simply one facet of that response.” Many other mammalian changes accord with the climatic episodes summarized in Sections 4.3.1 above. Examples include the increase in cursorial and migratory forms during major cooling trends (e.g., FADs during the start of the modern ice age of genera which today are migratory, such as Connochaetes in Alcelaphini [Vrba 1989a], Oryx among hippotragines [Vrba and Gatesy 1994], and the antilopine Antidorcas [Vrba 1995c]). Increased encephalization is linked to more advanced social organization and to life in more open, seasonally cooler and drier evironments, not only in Homo but also in other mammals (e.g., see Oboussier's [1979] results for EQ variation in a large range of living African bovids). An example of major modification of locomotory structure and function, convergently with what happened in hominids, is the evolution of bipedalism in rodents. As noted in Section 4.3.3 , the new species of micromammals which first appeared during the cooling trend after 2.9 Ma included several bipedal steppe- and desert-adapted rodent taxa (Wesselman 1995) such as the first African and global appearances of the genus Jaculus of desert gerboas and a springhare species Pedetes. Hafner and Hafner (1988) pointed out that the bipedal forms share suites of characters—including enlarged hindfeet, heads, brains, eyes, and auditory bullae—while many of them also have larger body sizes. According to these authors, this highly specialized rodent body plan and bipedal locomotion is today strongly associated with open, arid, mostly desert habitats, and appeared numerous times independently in rodents (in 24 genera in 8 families). The world wide fossil record of bipedal rodents (Lavocat 1978; Savage and Russell 1983; Wesselman 1995) suggests that most may have appeared during times of global cooling and land aridification either during the Late Miocene or the Late Pliocene.

4.4 Climate in relation to the evolution of ontogeny

4.4.1 Heterochrony pulses: parallel developmental responses to common environmental causes

The term heterochrony has been applied to both ecophenotypic and evolutionary changes in the rates and timing of ontogenetic events (Gould 1977). The same kind of heterochronic phenotype, H, commonly appears independently in different parts of a given monophyletic group in association with the same kind of environmental condition, E, and variously as an ecophenotype (i.e., reversible in later generations not faced by E) or as a phenotype, the expression of which is genetically fixed (or at least more constrained under varying conditions). An example is relative reduction of limb length in colder environments, an aspect of Allen's Rule (Allen [1877]: mammalian extremities are reduced relative to body size in cooler climates). Not only the environmental association with E but also the growth patterns tend to be similar between the independent occurrences of such a phenotype H in a clade (Gould 1977a; Wake and Larson 1987; Vrba 1998b). It appears that certain kinds of heterochrony are more likely than others under particular environmental changes. Each heterochrony response starts off from the ancestral ontogenetic trajectory for that character, and this inheritance imparts limits and direction on what can grow and evolve. To the extent that aspects of ontogeny are shared by common inheritance between related species and across larger taxonomic groups, similar kinds of heterochrony will evolve independently in related lineages faced by the same environmental change. A summary and extension of the above is given in the following two statements (Vrba 2004, 2005):
  1. 1.

    Similar environmental changes elicit similar heterochronies in parallel, potentially in numerous lineages across large phylogenetic groups. Such heterochrony often involves change in body size and may be accompanied by large-scale phenotypic reorganization (Arnold et al. 1989; Vrba 1998b) such that the parallel heterochronies involve concerted evolution of suites of linked characters and “shuffling” among body proportions.

     
  2. 2.

    At times of widespread climatic change, diverse lineages may show parallel changes in size and in similar kinds of heterochrony associated in time and consistently with the climatic change—a “heterochrony pulse.” “Pulse” here does not imply that the lineages responded in unison in a short time but only that the events are significantly concentrated in time.

     

I will mention one particular category of heterochrony, which is associated with body size increase by prolongation of growth and which is a common mammalian response to colder temperatures. It is of especial interest in the Plio-Pleistocene context of net global cooling; and it appears to have affected many African mammals including some evolutionary changes in Homo.

4.4.1.1 Cooling and body size increase

Many species with FADs during times of cooling and aridification were larger than their ancestral phenotypes (as cladistically inferred). For example, Vrba (2004) tested H 0 that size changes across lineages are randomly distributed in time in the Alcelaphini (wildebeests, etc.) and Reduncini (waterbuck, etc.), which together comprise 63 recorded species over the past 5 Myr with a body weight range of ca. 20–250 kg. The result of significant peaks in size increase over 3.0–2.5 Ma and 1.0–0.5 Ma, two periods with strong cooling, is consistent with Bergmann's Rule (1846: larger bodies are associated with colder temperature). While exceptions have been noted, in general the predictions are upheld in living mammals (Ashton et al. 2000; Meiri and Dayan 2003), including in humans (Baker 1988) and fossil mammals (Kurten 1959; Heintz and Garutt 1965; Davis 1981). To evaluate the claim that climate-associated heterochrony can involve extensive rearrangement—or “shuffling”—among body proportions, with parallel changes across related lineages, consider the example of Bergmann's Rule. Bodies can become enlarged by faster growth relative to the plesiomorphic (or directly ancestral) ontogeny, by prolongation of growth time, or by a combination of both; and the influential factors may include temperature change itself or one of the attendant environmental changes (such as seasonal changes in food and water availability [Guthrie 1984; Barnosky 1986]). Such changes in growth mode are expected to result in rearrangement of body proportions. This is especially true of growth prolongation which is prevalent among Bergmann cases for which there are growth studies. For instance, many African tropical ungulates have shorter growth periods to smaller size in warm lowlands, while their close relatives at higher altitudes and/or latitudes grow for longer and become larger. The example of polymorphism in the African buffalo was noted earlier: Syncerus caffer caffer is much larger (up to 810 kg), grows for longer, and lives at higher latitudes and/or altitudes always near grassland, while the smaller and plesiomorphic phenotype S. c. nanus (up to 320 kg) with a shorter growth period lives in warmer, more forested regions.

4.4.1.2 Body size increase and “shuffling” among body proportions

Consider what is expected under the simplest way in which growth prolongation could occur: namely, if all ancestral growth phases for a character become proportionally prolonged (or extended in time by a constant factor) while maintaining the ancestral number of growth phases and the ancestral growth rates for respective phases (Vrba 1998b: Fig. 1). Let us call that simple proportional growth prolongation. Characters in the same organism have differing growth profiles in terms of growth timing and rate in relation to age and body weight (Falkner and Tanner 1986); and character growth typically occurs in distinct phases in each of which character change is nonlinear with respect to age (Koops 1986). We can distinguish two major types of heterochrony and associated allometric growth under growth prolongation: (1) In type A heterochrony, characters which grow with net negative allometry with respect to age and body size will become reduced relative to body size in the adult stage of the prolonged descendant ontogeny (even if no other growth parameter changes) and paedomorphic in that the descendant adult resembles the ancestral juvenile. A probable example is character evolution by Allen's Rule (Vrba 1998b, 2004) which is upheld in modern humans (Baker 1988). The persistence of Allen's Rule in modern biology supports the general hypothesis of similar changes in body proportions across lineages, which share inherited developmental responses to common environmental causes. (2) In type B heterochrony, characters which grow with net positive allometry become relatively enlarged. This mode, particularly by prolongation of a positively allometric late growth phase, may be how the hypermorphosed antlers of the giant Irish Elk evolved (Gould 1974) and how exaggerated secondary sexual characters in enlarged bodies commonly evolve (Vrba 1998b). As growth trajectories become prolonged, some characters become relatively reduced and others enlarged, with potentially extensive rearrangement among body proportions and substantial evolutionary novelty (Vrba 1998b: Fig. 1). Type B heterochrony can also result from prolongation of positively allometric early growth in which case the descendant structure is relatively enlarged and paedomorphic. An example is provided by the enlarged hindfeet of the bipedal, saltatory rodents during times of cooling (Section 4.3.4 ). If the growth of rodents, the juveniles of which in general have relatively large hindfeet (Hafner and Hafner 1988), is prolonged, a descendant adult with enlarged hindfeet is predicted. Evidence for at least some taxa is consistent with this, e.g., bipedal Kangaroo rats, Dipodomys, which inhabit semiarid to arid regions in North America, have longer growth periods and are hypermorphosed in some characters—yet paedomorphosed in others—relative to the ancestral ontogeny (Hafner and Hafner 1988). As noted earlier, the bipedal forms share suites of characters in a characteristic body plan, which is today strongly associated with open, arid habitats and has appeared independently in 24 genera in 8 families (Hafner and Hafner 1988). I do not know how many of the 24 instances of parallel evolution involved growth prolongation. But I suggest that at least some of these appearances of suites of integrated character complexes exemplify coordinated morphological changes, by growth prolongation within and between lineages in response to a common climatic cause. This case illustrates that evolution by growth prolongation, as it acts on characters with different nonlinear growth profiles in the same body plan, can result in a “shuffling” of body proportions. Substantial novelty in form can result, and also in function, as in these rodents which can jump to a height that is from 4 to 25 times their body length. I next discuss another example of type B heterochrony with prolongation of positively allometric early growth, namely encephalization.

4.4.1.3 Heterochrony and brain evolution

I applied statistical models for multiphasic growth to data on living human and common chimpanzee brain weights at ages since conception to test the hypothesis that encephalization of the human brain occurred by simple proportional growth prolongation (Vrba 1998b). Specifically, I wanted to know whether prolongation of the fetal growth phases, with strongly positive allometric growth, could account for most of the observed EQ increase. The results supported the hypothesis and imply that gross brain weight increase toward humans required change in only one growth parameter: prolongation of the nonlinear ancestral growth phases. In mammals in general, simple growth prolongation is predicted to result in encephalization as all mammalian brains complete a large proportion of their total growth rapidly early in ontogeny (Count 1947; Holt et al. 1975). The association in other mammals not only of body size increase with cooling but also of encephalization with more open, seasonally cooler, and drier environments, has already been noted. This raises the hypothesis that there were past “encephalization pulses” across many mammalian lineages in response to cooling over particular intervals (Vrba 1998b).

4.5 Conclusions

Environmental stimuli have influenced the evolution of hominids and other mammals at the levels of ontogeny, organismal adaptation, and speciation. The linkages to hominid adaptation have received most attention and some agreement has emerged in this area: successive cooling trends since the Late Pliocene were associated with the earliest evidence of—and probably initiated—the “hypermasticatory trend” in Paranthropus (ca. 2.6 Ma) and its later exaggeration ca 2.3 Ma, stone tools and their use to butcher carcasses (ca. 2.6–2.5 Ma), Early Pleistocene expansion of tool kits, increased mobility by the Plio-Pleistocene interface and commitment to long-range bipedalism (ca. 1.6 Ma) in Homo, and significant brain expansion near 2 Ma and also since 600 thousand year ago. There is some consensus that encephalization and culture in Homo represent generalist adaptations which conferred a more flexible and expanded use of resources (Vrba 1989a; Potts 1998; Wood and Strait 2004). It now seems likely that the masticatory features of Paranthropus, while adaptations for consuming tough or gritty foods, had the effect of broadening, not narrowing, the range of food items consumed and allowed these forms to subsist in varied environments (Wood and Strait 2004). There is less agreement on environmental stimuli of the onset of bipedalism; in fact, doubt has been cast on the old “savanna hypothesis” by evidence ranging from locomotor anatomy of some early hominids to indications of dense tree cover in their environments. I discussed why, even if the hominid ancestor and its bipedal descendant species both live(d) in forest, this does not necessarily mean that climatic change did not bring about speciation.

Far less work has been done on the issue of environmental stimuli of hominid speciation. A brief summary of the current status is as follows: In terms of theory, the expectation that allopatric speciation predominates, particularly in hominids and other large mammals, is consistent with the weight of available evidence. It would take special pleading to argue that hominids are exceptions. If allopatric speciation predominates then so must physical initiation of speciation predominate. Most, and possibly all, of the hominid FADs either coincide with or fall very close to one of the major cooling trends. While taphonomic factors and chance may have contributed to this pattern, it does leave intact the hypothesis of climatic cause of hominid speciation. Also, on cladistic grounds, some speciation events must be closely associated with climatic change in hominids (Kimbel 1995) and other African mammals (Vrba 1995c). A study of the African larger mammal record of the past 10 Myr showed several turnover pulses which coincide with global cooling trends and that global cooling with increased aridity and seasonality was a more important stimulus of turnover than was global warming (Vrba 2000, 2005). A related finding is that since 10 Ma, the average large African mammal species started in a geographic distribution that was more restricted than later on (Vrba and DeGusta 2004), supporting hypotheses of speciation which emphasize the physical initiation of isolated populations.

Environmental stimuli of ontogenetic evolution have hardly been studied in our field. I discussed the “heterochrony pulse hypothesis”: the generative properties shared among lineages can result not only in coherence of morphological changes but also in a strongly nonrandom timing of heterochrony events, as diverse lineages respond in parallel by similar kinds of heterochrony to the same environmental changes. This has not yet been tested. Of particular interest in the present Late Neogene climatic context is heterochrony involving body enlargement by prolongation of growth, because it is associated with colder (at least seasonally colder) temperatures (Bergmann's Rule, upheld in modern humans [Baker 1988]). I have discussed some examples, including encephalization as a result of growth prolongation, in hominids and other mammals and have suggested that there were past “encephalization pulses,” across many mammalian lineages, in response to cooling trends over particular intervals such as during the onset and later intensification of the modern ice age.

In our field, one sometimes regrets (at least I do) that conclusive answers, such as emerge from some experiments of physical scientists, are so difficult to achieve. Hypotheses on the subject of environmental causes of hominid and other biotic evolution are difficult to test because the data come from different subdisciplines, each with its own set of biases and errors. As a result, debates tend to continue interminably. While we have a long way to go, on the positive side we can take heart in the simple fact that we are, so to speak, in a “growth industry”: while many aspects of life are deteriorating, the fossil record with its associated geological information is constantly improving. Thus there is a good expectation of future progress on some of the unresolved issues. In my view the results to date already offer support for the notion that common rules give qualitative and temporal coherence to the evolutionary responses across many mammalian—including hominid—lineages. These common rules arise from the regularities of physical change and from attributes of organismal ontogenies and phenotypes, and species, which are widely shared by common inheritance. The evidence implies closer linkages between the physical and biotic dynamics on earth than has traditionally been acknowledged. This perspective contrasts with a neo-Darwinian view: that selection of small-step random mutations is the vastly predominant evolutionary cause, with the implication that each evolutionary advance is to a larger extent an independent piece of history. Evolution is more rule bound than that, and our evolution is no exception.

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