The evolution of innateness has been one of the oldest and most mysterious problems in evolution (Lamarck 1809; Darwin 1859; Duerden 1920; Waddington 1942; Lorenz 1966). We have seen the evolution of innateness at the genetic level in the cases of gene fusion and the evolution of alternative splicing patterns, and we will now see it at the organismal level. Although the empirical facts to be discussed are known, they have not yet been used to make a new argument about the nature of the evolutionary process. I will focus on examples from the evolution of behavior, thus complementing past literature on novelty, which has focused on morphological evolution (Müller 1990; Müller and Wagner 1991; Müller and Newman 2005; Moczek 2008; Wagner and Lynch 2010; Hall and Kerney 2012; Hallgrímsson et al. 2012; Peterson and Müller 2013).
I will first cover innateness from multiple angles in Sects. 4.1–4.11, and then discuss the emergence of novelty in detail (Sect. 4.13). We will see that improvement, innateness, novelty and stabilization all come together as different aspects of one process. At the end of Sect. 4, both the consistency with past literature on novelty and the contributions to it will be clear (Sect. 4.16). Readers interested in the molecular level may note that it will be revisited in Sect. 5.
The Problem of the Preexistence of High-Level Mechanisms
The ability of pointer dogs to point at the prey in a statuesque manner is to a large degree innate (Arkwright 1902). How did this instinct evolve? To argue that a sequence of random mutations of small effects has built up the behavior from scratch such that it has always been instinctive and never learned is unappealing: Would breeders have recognized slight inborn tendencies to point at the beginning of the evolutionary process involved and, without regard for the outcome of any training, base their artificial selection on these differences? And if training were important in the evolution of pointing, one may expect that the highly evolved abilities of the animal to learn would have masked out presumed mutations of slight effect for an independently developed instinct. All would be much more understandable if we consider that a trait that previously required learning through reward and/or punishment has become emancipated in the course of evolution from these external cues.
Consider the evolution of migration. In an instinctive and automatic manner, a young common cuckoo (Cuculus canorus) takes off in the fall from its breeding grounds in Scandinavia, flies thousands of miles to its wintering site in Central Africa and then returns in the spring (Willemoes et al. 2014). How did this complex suite of instincts get started in evolution? Both Darwin (Romains 1883) and Wallace (1874) hypothesized that the breeding and wintering grounds gradually became separated and the distance between them increased; that originally, the animals were tracking seasonal changes in resources over short distances as a direct response to the environment; and that in time this behavior became habitual and instinctive (Romains 1883; Wallace 1874; see also Woodbury 1941). To assume that the migratory instinct evolved afresh, independently of the behavior that came before it, brings up the same problem as in the case of the pointer dogs: the pre-existence of an evolved, general-level mechanism (in these cases, the brain) that is able to respond adaptively to environmental changes and was presumably involved in the original phenotype.
In an experiment designed to capture the evolution of innateness (Waddington 1953) (see also Waddington 1956, 2006, 1959; Bateman 1959a, b), Waddington took Drosophila melanogaster flies and exposed their pupae to a heat shock. As a result, a fair number of the flies that developed showed a particular vein pattern on their wings called “crossveinless”.Footnote 15 He then bred the crossveinless flies to form the next generation of the experiment and repeated this procedure of heat shock and selective breeding over the generations. As a result, the percentage of crossveinless flies increased over the generations and, beginning at generation 14, a small percentage of flies started showing the new vein pattern without exposure to heat shock, that is, innatelyFootnote 16 (Waddington 1953). The intriguing experimental outcome was that this trait became innate, even though no selection for such innateness was performed.
To explain this outcome, called “genetic assimilation” (Waddington 1953), Stern (1958) (see also Falconer 1960) proposed a model based on traditional principles. The model assumes the preexistence of alleles that make independent contributions toward a certain sum, such that if the sum surpasses a certain threshold, the trait of interest is exhibited. Furthermore it makes certain assumptions about the initial frequencies of alleles and the normal and experimental conditions thresholds that make it so that, prior to selection, the trait of interest (e.g., crossveinless) is exhibited in practice only under experimental conditions (e.g., heat shock), whereas post selection it is exhibited under both experimental and normal conditions, and thus the trait can be said to have become innate. However, despite the mathematical crispness of this model, taken literally, it means that every trait that is to become innate has its own set of additive alleles that preexist and provide the potential for that trait to become innate as is. That is, there are additive alleles that, if they surpass a threshold, build a brain that points, and there are different sets of additive alleles lying dormant in birds for every possible migration route, such that each set builds a brain for a particular route if it surpasses a certain threshold.Footnote 17 Indeed, Waddington himself rejected this model (Waddington 1958, 1961), because it did not apply to the complex natural cases that motivated the problem. Here, I will provide another explanation for innateness based on interaction-based evolution.
Modularity and Innateness are Caused by Simplification
As Waddington (1942) alluded to, when an emerging module is released from the influence of an element inside the organism, the result is seen as modularization; and when it is released from the influence of an environmental factor, the result is seen as the evolution of innateness. In Sects. 2.2 and 3.1 I argued that simplification is connected to modularity and innateness: the formation of modules streamlines the developmental process and involves emancipation of an emerging module from complex influences, both internal and external. Indeed, simplification leads to modularity and innateness.
Approaching the topic of innateness equipped with the theory of gradual network change presented here, it is useful to distinguish between two important phenomena that I will call “emancipation” and “acceleration.” Emancipation refers to the fact that units (modules or elements) can be copied and the connections between units can gradually evolve such that a unit can be subjected to different regulation than that of its source copy. Acceleration refers to the idea that the coming together of units under one control simplifies development locally while absorbing novel phenotypic meaning from the changing context. Both these aspects of network level evolution, discussed in Sect. 2.2, will be clarified here with the help of examples, and both figure into the explanation of innateness to be given in the following sections.
The Evolution of Innateness is More Common than We Realize
In an idealized view of the crossveinless experiment, we can think of the crossveinless trait as qualitative (present or absent) and assume that it is the same in the beginning of the experiment as it is at the end. The only thing that evolves under this assumption is the propensity to produce it. In this case, we may simply use the word “emancipation” to describe what happens to the crossveinless trait when it comes to appear without the environmental trigger. But crossveinless is an extreme, chosen for its simplicity. In nature, when the evolution of innateness or emancipation takes place, the trait that is to become innate also evolves at the same time. For example, in cases of ritualization, a non-signaling behavior is gradually released from its context and becomes used as a signal (e.g., an egg-fanning movement becomes a showing-the-nest signal, Tinbergen 1951; see Sect. 4.6) (Huxley 1914; Whitman 1919; Armstrong 1950; Tinbergen 1952). As Tinbergen noted, those ritualized traits that are emancipated are usually traits that have already changed much from their original form; and we would not have been able to make a connection between the signal and its origin if it were not for the fact that, at least in some cases, there happened to be a transitional series betraying the connection between the two, such as in the threat posture of the Manchurian crane (Grus japonensis) (Lorenz 1935; Tinbergen 1952). In other words, there exists a continuum of differences between the non-innate ancestral and the innate derived traits, that ranges from no difference, to a great difference that obscures the connection between the ancestral and the derived; and cases at the former end of the spectrum are rare.
I argue that this is precisely the problem with observing innateness. Darwin and other early naturalists believed that what is habitually performed due to environmental triggers over the generations gradually impresses itself on the hereditary constitution of the species and becomes innate and emancipated from the environment, and that this is explained by the laws of use and disuse, or Lamarckism (Romains 1883; Darwin 1859). I argue that such automatization does happen in general but is often hard to see because of the difference between the ancestral and derived traits, and that it is network-level evolution and not Lamarckism that is responsible for it.
Evolution of the Whole as a Whole in Innateness
The fact that a trait changes as it becomes innate allows us to examine the evolution of a complex whole, while involving not only emancipation but also fusion and acceleration.
While I have been using the term “innate” without qualification so far, it is useful to note that there is no strict separation between the innate and the non-innate. Learning itself is enabled by instinct (Lorenz 1965; Gould and Marler 1986). No trait develops in a manner that is independent of the innate nature of the organism, and no trait develops entirely independently of the environment, when the latter is broadly construed (Lehrman 1953). Therefore, rather than speaking of “innate” and “non-innate,” we realize that there is a continuum between traits developed more directly and quickly (“innate”) and traits that require more unfolding that involves more interactions with the environment.
When we consider this continuum as it applies to a given organism, we should consider that it evolves as a whole—the process of development evolves as a whole. Then, we can bring the ideas of gradual network evolution to bear on it (Sect. 2). I argue here that the evolution of innateness arises as a result of the “chunking” or modularization of a previously complex part of the network—what were previously independent elements each under a different control have now become simplified or combined into a singe unit. Although it may seem that this simplification accelerates development in the course of evolution toward the final trait, in general, development is not accelerating toward the final trait as it was before, but rather toward what that trait has in the meantime changed into, and therefore nothing is being accelerated strictly speaking. Therefore, it is the signature of the previously less innate that we generally see in the current more innate, rather than a direct facsimile. There is no Lamarckian transmission that takes a developed or a learned trait and makes it innate. As argued in Sect. 2.2, to use a metaphor, in an Archimedes screw, water is moved along the shaft even though each point in the screw only rotates at its own level. So in evolution, the non-innate does not itself become innate—the phenotypic does not become genotypic—but rather evolutionary action at each level of biological organization takes place within that level, while accelerating development.
Indeed, we know that the adult form influences the evolution of the earlier stages of development: there is selection on the adult form, and therefore there is selection on earlier stages of development to lead to a well-performing adult. When considered from a traditional standpoint, this trivial point turns into a problem because development is a complex process, and traditional evolutionary theory is not equipped to deal with a complex process. Traditional evolutionary theory cannot conceive of a complex evolutionary change that modifies the developmental process as a complex whole: it does not have a sense of accelerationFootnote 18 or an emphasis on emancipation, and therefore when a trait appears earlier in development that seems to relate to one that used to come later in development (e.g., innate migration relates to earlier, learned migration), it absurdly has to invoke an evolution of that trait afresh, absent any connection to that which it obviously relates to. While Gould attempted to address this problem, he did so by breaking the whole again into parts and arguing that the timing of appearance of one part or a developmental process in and of itself can be moved earlier or later in development (Gould 1977), which is a very limited explanation that does not address the range of phenomena discussed here.
I have presented, in contrast, a view of the evolution of the whole as a whole. Instead of the evolution “afresh” idea that arises from a traditional perspective, this view raises the notion of acceleration as described: The quicker arriving at an evolving developmental outcome has the appearance of the evolution of innateness, thus involving interaction-based, network-level evolution in innateness. We have seen this in the case of the TRIM5-CypA fusion and the evolution of alternative splicing patterns at the molecular level, and will see it now in many examples at the organismal level.
Example: Pointing in Pointer Dogs
Pointing in pointer dogs will serve as an example of the importance of the evolution of the whole as a whole in innateness. I propose that selection has operated on the outcome of the training, favoring hunting dogs whose behavior following training was more pleasing to their owners, specifically in stopping upon discovery of the prey instead of chasing it further. However, since innate tendencies guide the learning, this selection has operated indirectly on innate tendencies, favoring dogs with the right set of innate tendencies that were more naturally inclined to learn the right behavior. In particular, I hypothesize that there exists among animals a widespread tendency to heed sudden changes; that in pointer dogs, this tendency has been strengthened in the course of evolution, in particular by heightening nervousness; and that other instincts have become at the same time adjusted to direct it productively, helping the dogs to learn to pause and freeze at the sight of prey. Over the generations, the learning task has become more and more natural to the dogs, and the amount of learning required has decreased, until today, the dogs require only minimal training, and they sometimes point at objects innately without any learning, as Darwin observed (see F. Darwin ed. 1909). Thus, selection for an improved outcome of the learning was accompanied by an acceleration of the learning and, ultimately, innateness. This hypothesis already has the advantage that it explains not only the evolution of the pointer dog instinct complex but also the nervousness syndrome that often afflicts these dogs: heightened nervousness helps them heed sudden changes, and when not properly compensated for results in the nervousness syndrome. Note that, while Grandin and Deesing (1998) argued before that pointing relates to nervousness, their discussion seems to assume that pointing and nervousness are traits with separate genetic causes that happen to be connected through genetic linkage, which suggests a spurious connection. In contrast, the hypothesis proposed here connects pointing and nervousness at a deep level, with the help of the holistic view of interaction-based evolution. There are no genes dedicated to pointing per se: pointing is a system-level phenomenon that emerges from a suite of interacting instincts and learning.
In an exceptionally inspiring chapter, Papaj has already argued that what is at first learned, over evolutionary time can come to be learned more quickly until it eventually becomes innate (Papaj 1993). In this respect, his hypothesis is similar to the above. However, lacking the ideas of interaction-based evolution, and treating instinct and learning as separate elements, he tried to create a model of a traditional kind, and admitted that the model failed to provide an explanation, because the evolution of innateness came out of an artificiality built into it (Papaj 1993). In contrast, the hypothesis presented here allows us to preserve Papaj’s intuition but in a natural way: it holds that selection has affected interacting instincts that guide the complex process of development and learning through a process of network-based evolution, and network evolution in turn involves acceleration and emancipation—an increase in the innate abilities. In addition, interaction-based evolution also explains why innateness and stereotypy are deeply intertwined (see Sects. 4.10, 4.11), which Papaj admits his model does not (Papaj 1993).
To reiterate, I propose that the process of evolution toward a better outcome of the learning leads at the same time to a quickening of the learning and that ultimately, a new innate trait appears, because what enables the organism to reach a better outcome through learning is that it is naturally inclined in the right direction. The organism “gets it” more, naturally and inherently, because underlying interacting instincts are being shaped. Thus, improvement comes together with innateness.
Importantly, the evolutionary process that shapes the network of underlying instincts can be seen as uncovering better “principles” that guide the learning (and more generally, development)—emerging underlying elements that organize a preexisting complex more simply. Consistent with Sect. 3 and with later sections (see Sect. 4.13), viewing things in terms of such principles leads us to a new prediction regarding novelty: the evolution of the new innate and the new and improved adult form will come together with the production of new, beneficial things that were not selected for in and of themselves but arose as corollaries or windfalls of figuring out the right principles. Improvement, innateness, and generalization—or the emergence of useful novelty not selected for—come together. As an example, backing in pointer dogsFootnote 19 may have evolved as a “corollary” of pointing—an unintended but desirable outcome.
Elements of Network Evolution: Chunking, Duplication, Emancipation, Cooption and Rigidification
As noted, ritualization is an evolutionary process that occurs when a behavioral element is gradually emancipated from its original use as it becomes coopted for use as a signal in the course of evolution (see, among other sources, Huxley 1914; Whitman 1919; Armstrong 1950; Tinbergen 1952 and further references below). For example, when a bird is about to hop or take flight, it bends its legs, lowers its breast, raises its hind parts and sometimes its tail, folds its neck and brings its head back almost to the shoulders, while slightly expanding its wings, so that the whole body is like a tight spring ready to be released for jumping, at which instant the legs straighten, the breast and hind parts line up with the direction of the jump, and the neck is stretched forward (Daanje 1951). Daanje argued that, from this movement, various signals have evolved. For example, when the male turkey displays to the female, it raises the hindparts a bit, raises and spreads its tail, folds its neck and brings its head back almost to the raised back feathers, and partly spreads its wings downwards. This posture imitates that of the jump in several elements, except that the legs are not bent, the tail and wing movements are exaggerated, and the posture is kept frozen for a while (Daanje 1951). Thus, a behavioral pattern which is widespread taxonomically and which originally had a mechanical function has evolved into a signal that is expressed in new contexts independently of the context of expression of the ancestral trait.
Another example of ritualization is the way that the male three-spined stickleback (Gasterosteus aculeatus) shows the nest entrance to the female. According to Tinbergen, this movement was derived from the egg fanning movement (Tinbergen 1951), which again demonstrates a shift from one context to another.
As we have just seen, ritualization requires emancipation from one context and cooption to another. Critically, these are operations of network evolution. The gradual release of an element from one context concomitant with the subjecting of it to another context involves two aspects of the organism at once and is inherently an interactive operation, well-described by modules moving in a network.
Baerends’s work on nest building, egg laying and offspring provisioning in the sand wasp Ammophila adriaansei (campestris) (Baerends 1941) demonstrates clearly that behavior is underlain by a network of modules. A normal behavioral sequence of the wasps is as follows: Build a nest; close the entrance temporarily with soil; fly away and hunt a caterpillar; carry the paralyzed caterpillar back; reopen the nest; put the caterpillar in; lay an egg; close the entrance again, this time with greater care. Now build another nest and repeat the entire process so far. Now return to the first nest; open the closure; make an inspection visit. If the egg has hatched and the nest is in order, close the entrance, and now bring 1-3 caterpillars in succession. Repeat this second phase for the second nest. Now return to the first nest, open the closure and make an inspection visit. If all is in order, bring 3-7 caterpillars in succession; then make an especially careful final closure of the nest entrance. Repeat this third phase for the second nest. Now build another nest, and repeat all from the beginning. Furthermore, if, in the first inspection described above, the egg has not hatched, the wasp may build another nest at that time. It can manage 4 nests at a time, with offspring at different ages at each nest requiring different amounts of provisioning (based on information obtained in inspection visits). If a nest has been disturbed, the wasp may abandon it.
A computer programmer would instantly recognize that the sand wasp’s behavior is an algorithm with subroutines (see flow chart in Fig. 1). The most parsimonious description of this behavior involves activation of the same behavioral modules or subroutines, such as “carry a caterpillar to nest” or “perform an inspection visit” in different contexts, and the different contexts, namely the different stages of laying and provisioning, themselves consist of different combinations of lower-level behavioral modules (Lorenz 1981).
Interestingly, Tinbergen wrote that the process underlying emancipation was not known, though it must somehow involve natural selection (Tinbergen 1952). The present theory highlights how correct he was to emphasize that unknown. At once we can understand the inability of traditional evolutionary theory to explain and connect with classical ethology: A network is defined by interactions. The evolution of a network is the evolution of a complex whole. The conceptualization of evolution based on traditional theory encouraged a one-trait-at-a-time type of thinking and was not suitable for discussing network evolution and the transfer of an element from one context to another (Gould and Vrba 1982; Gould 2002). Importantly, Tinbergen also noted that there is no point during emancipation at which a behavioral element stops belonging to its original function and starts belonging to a new function (Tinbergen 1952). Rather, as in the verbal model of network evolution discussed in Sect. 2.2, the change of context and meaning is gradual.
Let us now think about the evolution of a network such as described by Baerends. Obviously, elements were not added to it in the form in which they exist today. For example, the construction of a well-shaped nest with a cell at the end had been preceded by a less involved modification of the environment. Also, elements were not appended in the course of evolution at the end of the behavioral sequence. That is, if “build nest”, “make closure,” “hunt caterpillar,” etc., are denoted a, b, c, etc., then it is patently obvious that the stages of evolution did not proceed in the following sequence: a, ab, abc, etc., or else absurdities arise such as not laying eggs until a certain point in evolution, performing an inspection visit before the existence of a foraging stage where information from this visit is used, etc. This means that the behavioral sequence was reorganized in the course of evolution and/or new elements were added at internal positions in the sequence. It follows that elements that came after positions into which new or preexisting elements were inserted, or from which preexisting elements were removed or translocated, must have been emancipated from their previous triggers (namely the completion of the behavioral steps that used to come before them) and subjected to new triggers (the completion of the behavioral steps that come before them now). Finally, we would not assume that each repeating element or subroutine evolved afresh in its entirety for each instance in the sequence in which it is used. This means that there has been a copying of routine calls, or, to use more generic terms, copying and differentiation of modules. Thus, operators of network evolution—emancipation, cooption, copying and differentiation of modules—have been involved in the evolution of sand wasp behavior.
Another example showing the insertion of elements at internal points in a sequence and sequence reordering is Lorenz’s study of display sequences in surface feeding ducks (Lorenz 1958). Lorenz found about 20 behavioral elements, of which different combinations make different display sequences in different species and even within the same species. Lorenz (1958) describes the study of three different species, the mallard, the European teal (Anas crecca) and the gadwall (Anas strepera), which share the following 10 elements:
He then presents some display sequences (where one element follows another in quick succession) for each of the three species. For the mallard:
For the European teal:
For the gadwall:
(the semicolon mark between sequences 5,6 and 10,6 in the gadwall means that they are fused at high excitation, which suggests, by connection with many other observations, that we are observing them in the midst of a process of evolutionary fusion; Lorenz 1958).
The sequences above are obligatory and innate. Hybrids produce their own sequences. This clearly shows network-level evolution in the sense of reorganization of modules, emancipation and fusion at the level of sequences of fixed action patterns (FAPs).
Critically, this example and the previous ones show us that the picture that we obtain by looking closely at evolution at the phenotypic level mirrors what the molecular biological and genomic revolutions have taught us about the genetic level: at both the molecular and organismal levels, network-level evolution is key (Wagner and Lynch 2010; Lynch et al. 2011, 2015; Müller and Wagner 1991; Hallgrímsson et al. 2005; Müller 2007a; Moczek 2008; Schlosser 2015). And network-level evolution is much better understood with the help of the principles of interaction-based evolution, including cooption, emancipation, acceleration and simplification.
Fusion, like emancipation, is also a network-evolution operation. While Baerends’s and Lorenz’s examples above demonstrate it at the level of sequences of FAPs, fusion can also generate elements at a lower level, namely the level of the single FAP; though—again mirroring the genetic level (see discussion in Sect. 2.4)—there is no sharp boundary between the single FAP and sequences thereof. One telling example was the inciting ceremony in ducks (Lorenz 1941/1971, 1958, 1966) described in Sect. 2.1: The movements of threatening the neighbors with the neck and of returning to the mate, originally triggered by separate environmental stimuli, have gradually fused over the course of evolution into a stationary neck-over-the-shoulder display triggered as one, while becoming emancipated from the presence of neighbors. These movements originally constituted territorial behavior, with an indirect, implied meaning of pair-bonding and team work; and as they fused, the pair-bonding meaning crystallized and moved to the fore (Lorenz 1941/1971, 1958, 1966).
Many related examples exist. The tendency to attack a neighbor when in one’s own territory and flee from the neighbor when in the neighbor’s territory is indeed a very general one, spanning birds, fish and mammals. In some fish, the neighbors exchange chase and be-chased turns, coincident with crossing the territorial boundary (Lorenz 1981). In the fire-mouth cyclid, Cichlasoma meeki, this chase and be-chased movement has become a highly rhythmic oscillation—it has become stereotyped. The fusion of the previously separately triggered back-and-forth movements in this species is revealed when one fish suddenly loses interest and disengages yet the other continues oscillating (Lorenz 1981). Evolution, in this sense, is a process of automatization.
Generalizing Beyond Ritualization: The Automatic Nature of Instinct
The following examples not only show that fusion and other elements of network evolution extend beyond ritualization but also demonstrate the automatic nature of instinct. Consider, for example, the pecking instinct in domestic chicks. This fixed action pattern (FAP) is present at birth and consists of three main elements: lunging the head, opening and closing the beak, and swallowing (Lehrman 1953). Since we would not assume that these three elements of the fixed action pattern have each evolved from scratch in the context of this FAP, we are forced to assume that they have been fused.
The classic example of a FAP—egg rolling in the greylag goose (Anser anser)—also shows fusion. Upon seeing an egg placed by the side of its nest, the goose stretches its neck in a particular fashion, places its beak over the egg, and then slowly rolls the egg back into the nest while performing balancing sideways motions with the beak to prevent the egg from slipping from the side (Lorenz and Tinbergen 1938/1970). This seems like an insightful sequence of operations, but in fact, when the egg is quickly pulled out from under the beak while in motion, the goose will continue to roll the remaining nothingness all the way to completion and tuck it under (Lorenz and Tinbergen 1938/1970), again showing the automatic nature of instinct.
Indeed, it is implicit in Barlow’s definition of the FAP that the FAP is a fusion of elements in general (Barlow 1977). Barlow defined the FAP (which he renamed “modal action pattern,” MAP) as a behavioral module usually indivisible but made of elements that appear individually elsewhere. It is quite informative that Lorenz (1958) had suggested that “perhaps all behavioral patterns” arise from fusion such as seen in the inciting example.
Ritualization Shows All Elements of Network Evolution in One
Interestingly, a single case of ritualization often exemplifies multiple or even all of the following characteristics: emancipation (also: routinization, autonomization, or evolution of innateness), cooption, fusion (chunking, or welding), increased efficiency, exaggeration (or “caricaturization”), schematization, simplification, stereotypy, automatization and rigidification (Huxley 1914; Whitman 1919; Armstrong 1950; Tinbergen 1952). Traditional theory has only offered to explain one or another of these phenomena in separate from the others. For example, Maynard-Smith and Harper (2004) suggested that stereotypy evolves because it standardizes competition. This suggestion not only ignores the fact that stereotypy exists also in non-signaling instincts where such competition is absent, but also ignores the common co-occurrence of the many elements above-mentioned. In contrast, the principles discussed in this paper unify these observations under one umbrella, as outlined below:
Emancipation: Emancipation (the release of a module from previous influences), or the evolution of innateness, is clearly demonstrated by the examples above, and has been addressed here as a part of interaction-based (or network-based) evolution. The same is true for chunking—the fusion of modules—which is also a part of network-based evolution.
Simplification: A fundamental concept in ethology is that of the “sign stimulus”—the stimulus that elicits a FAP. “Sign” means “simple”: the sign stimulus obtained its name from the fact that the animal attends only to a very limited part of the situation that we know it to be capable of perceiving through its senses. It attends to a parsimonious summary of the situation—a key. Yet the simplicity of the key is only relative: it is still a complex whole, a pattern involving relations between elements (Tinbergen and Kuenen 1939; Lorenz 1939; Krätzig 1940; Tinbergen 1951). For example, the gaping response of nestling Turdus merula as soon as they open their eyes can be directed at a model consisting of a mere three discs that touch each other. However, it is preferentially directed toward one of the discs that bears the right size-relation to another disc, such that the two together can be interpreted as a simplified schema of head and body (Tinbergen and Kuenen 1939). As another example, an abstract cross-like model (including symmetrical anterior and posterior “wing” edges, and central short and long protrusions perpendicular to them) elicited an escape response from young birds, but only when it was moved in the direction of the short end of the cross, as only in this case the short end can be interpreted as a short neck, which is the case for birds of prey (Lorenz 1939; Krätzig 1940; Tinbergen 1951). In other words, an abstract combination of elements is the evolved key. Now, Tinbergen argued that evolved rituals, which are themselves stimuli eliciting behavior in others, have been “schematized” through evolution and are evolved sign stimuli (Tinbergen 1952). Thus, in retrospect, his statement is consistent with the claim made here that rituals (and I will add the reception of signals, the “innate releasing mechanism,” or IRM; Lorenz 1981) have been evolutionarily simplified under performance pressure to their complex essence.
Exaggeration (or “caricaturization”): Ritualized signals are often exaggerated, as in the case of throwing the neck over one shoulder and then the other during inciting in the golden-eye (Sect. 2.1). Although it has been suggested that exaggeration has evolved under natural selection for visual clarity, one may ask whether organisms really need such a degree of clarity.Footnote 20 I argue instead that exaggeration is related to “caricaturization” or “schematization” (terms used in the literature) and the final touch of perfection (Sect. 3.1), and evolves by active simplification under performance pressure (Sect. 3), not by minute economical considerations.
Stereotypy: Stereotypy—or the lack of variation between individuals in a certain trait, or even between different instances of the behavior in the same individual—is another prominent aspect of rituals. According to interaction-based evolution, stereotypy is an inherent aspect of evolution, as will be discussed in Sect. 4.10.
Cooption: Cooption is inherent to Tinbergen’s definition of ritualization, as noted (a non-signaling behavior is coopted as a signal) and is also a crucial part of interaction-based evolution.
Thus, interaction-based evolution provides a more parsimonious view of ritualization than traditional theory. This provides both additional support for interaction-based evolution and an improved conceptual understanding of ritualization.
Recapitulation: Network Evolution and Phenotypes
In the model of network evolution (Sect. 2.2), I argued that two genetic elements that previously were regulated by two separate lines of controls and had to be separately expressed before coming together in an interaction can, over evolutionary time, gradually come together under one control and even fuse to form a new gene. In this process, there is not only emancipation (since one or both of these elements is emancipated from what previously controlled it) but also a sense of automatization, innateness and acceleration, as the emerging unit is no longer constructed from its elements by developmental interactions but rather has been evolutionarily accelerated into a ready-made unit or gene. We can now see that, like the genetic-level examples, the organismal-level examples that demonstrate emancipation and cooption also demonstrate the evolution of innateness, automatization, and acceleration, as expected. In the pecking instinct of domestic chicks, for instance, the lunging of the head, the opening and closing of the beak, and the swallowing, have been fused together. Therefore, the last two elements follow the first one automatically now, even though they must have been originally triggered separately by the environment. Furthermore, this welded instinct appears soon after hatching, and perhaps even in the embryo to some degree (Lehrman 1953; Kuo 1932a, b), demonstrating the evolution of innateness and acceleration. Similar points can be made, for example, about egg rolling in the greylag goose or the inciting ceremony in ducks (Sect. 2.1).
Stereotypy and the Evolution of Complex Phenotypes: The Process by Which Phenotypes Become Fixed
Interaction-based evolution argues that selection evaluates individuals as complex wholes (Livnat 2013). Unlike selection on additive variance (Fisher 1930), it argues that genetic interactions are at the core of the adaptive evolutionary process. Unlike the shifting balance theory (Wright 1931, 1932), it argues that genetic interactions are not formed by random genetic drift but rather transient genetic combinations are continually subject to selection. This kind of process has not yet been modeled mathematically. However, Livnat (2013) has made the following verbal argument regarding it. If selection acts on transient, complex combinations of interacting alleles across loci, then the information relevant for adaptive evolution under selection must be non-local: adaptive phenotypic change does not appear first in one individual and then spread to all, but rather forms at the population level through the concomitant spread under selection of many interacting alleles across loci (Livnat 2013). As some alleles spread in the population to fixation, the phenotypic variation that used to be caused by the sexual shuffling of these alleles must also gradually disappear, and thus, with regards to this variation, individuals must gradually become more similar to each other over the generations (Livnat 2013). This implies that stabilization accompanies the evolution of adaptation in general, rather than requires a separate force for stabilization of a trait per se, implemented by accidental mutation and natural selectionFootnote 21 (Stearns 2002). I called this effect “convergence” at the population level (Livnat 2013) (note that this usage of the term is distinct from the usual meaning of convergence in evolution).
If this is correct, then we should see a continuum of phenotypic fixedness corresponding to the formation of traits, with different traits lying at present at different points along that continuum. Some traits, still early in the process of formation, will appear as less stable or stereotyped, and others, at later stages in the process, will appear as more so. Thus, under interaction-based evolution, stereotypy can be seen as an indication of the degree of evolutionary progress of a trait.
An example is provided again by the pointers. Darwin wrote that the hunting behaviors that characterize the pointers are basically innate, and that the only difference between them and “true instinct” is that they are “less strictly inherited” in that there is variation in the individuals’ “degree of inborn perfection” and therefore in the extent to which they require training (Romains 1883, p. 237). Indeed, pointing in a statuesque manner, backing other dogs and other hunting-relevant behaviors have all been observed to occur often in pups that have not had the opportunity for learning by instruction, imitation or experience, and they are not exhibited immediately or to the same degree in all pups (Arkwright 1902). When training is required, the amount of training required is small: the trainer only guides the dog toward expressing what it already has a strong natural tendency to express (Arkwright 1902). The existence of variation in pointing behavior becomes natural from the perspective of interaction-based evolution: if traits evolve from fuzzy to sharp, if they are gradually stabilized, as discussed by Livnat (2013), then this simply means that pointing is still in the process of formation and has not yet become perfectly innate.
In light of the above, interaction-based evolution provides a distinctly different view than the traditional one on the evolution of stereotypy. Those who previously tried to explain stereotypy argued that signals must be clear, that stereotypy makes them clearer, and that they are selected for this extra clarity in a traditional process of selection (Mayr 1974; Barlow 1977).Footnote 22 However, I argue, first, that the clarity-based approach lacked parsimony from the beginning, because stereotypy is a property of instinct in general, not just of signaling behavior specifically; and second, that the clarity-based approach is unnecessary: the degree of uniformity is an outcome of the temporal nature of the process. This degree is in general associated with the point that the trait has reached along the spectrum of formation, and we observe that it varies across traits because we are witnessing traits at different stages of formation. Even if uniformity per se can be of value, the traditional focus on uniformity as a separate end obscures the general point: stabilization is not in and of itself a separate target of selection as traditionally perceived; it is an inherent part of interaction-based evolution.Footnote 23
Hinde’s comparative study of displays in finches demonstrates several of the points above (Hinde 1955). First, the same trait may vary more or be more stereotyped in one species than another. Second, demonstrating the evolution of FAPs from interactions, most displays in the finches studied by Hinde are not yet fixed action patterns but rather are poses whose elements tend to occur together statistically. Third, of the different displays, the one which is particularly rigid, stereotyped and emancipated (the female soliciting posture), is also the one that is far more widely shared, and therefore more ancient, than the other, still variable displays, in accord with the prediction above that stereotypy is indicative of the evolutionary stage of formation of a trait. Another, in-depth example showing the evolution of different degrees of fixedness, and that stereotypy is a concomitant of the evolution of adaptation—the evolution of decoy-nest construction in sand wasps—will be given in Sect. 4.12.
Interaction-Based Evolution Provides a Single Explanation to the Different Aspects of Innateness
“Innate behavior” or “instinct” has been used to mean different things in the literature (Papaj 1993):
Independence: It has been used to refer to behavior that is independent of interactions with the external environment like learning or experience. Such independence is especially clear when a behavior is present from birth, as for example in the pecking of domestic chicks (Lehrman 1953).Footnote 24
Stereotypy: Innate behavior has been referred to as stereotyped (also, “fixed,” “constant,” “rigid” —“robotic;” Papaj 1993).
Sharedness: Innate behaviors have been found to be homologizable between species and therefore useful for taxonomy. In other words, they are shared between species, with some species-specific characteristics (Lorenz 1981; Heinroth 1911; Whitman 1898, 1919).
The fact that these three aspects are connected empirically is clear.Footnote 25 But why are they connected? Tinbergen’s tone regarding the empirical connection between points 2 and 3 above was that of surprise (Tinbergen 1951, p.191). Barlow discussed stereotypy in the context of the clarity of signals (Barlow 1977), which neither addresses stereotypy in non-signaling behavior nor explains the connection between stereotypy and independence. And Papaj’s model was unable to connect stereotypy and independence (Papaj 1993).
However, interaction-based evolution connects the different aspects of innateness. First, traits evolve by a process of convergence as defined (see Sect. 4.10; Livnat, 2013)—a process of stabilization which begins at a state of high variance and eventually leads to the evolution of uniformity and therefore stereotypy (Livnat 2013). Since this process takes time, it makes it so that stereotyped elements are older and more widely shared than elements not yet stereotyped, while implying that stereotypy evolves across related species in parallel. This point connects the sharing of a trait between species with stereotypy (aspects 3 and 2 above, respectively).
Second, I have argued that interaction-based evolution works in the long-term through simplification under performance pressure. This can not only make one intra-organismal module independent of another, but also make it independent of environmental factors (see Sect. 4.2). Therefore, the process of interaction-based evolution leads not only to stereotypy but also to increased independence from environmental factors (1). This ties together independence, phylogenetic sharedness and stereotypy.
Interaction-based evolution also explains two other important aspects of innateness. One is that the fixed action pattern (FAP) often and perhaps always consists of fused elements (Lorenz 1958) (see Sects. 4.6, 4.7), which aligns with the fact that fusion is an outcome of network-level evolution. The other is the issue of circuitous vs. accelerated development, which will be discussed later (see Sect. 4.14), and which will clarify the connection between evolution and learning.
Evolution from Fuzzy to Sharp: Examples of the Evolution of Complex Phenotypes
In this paper, we have seen that examples of the evolution of complex phenotypes fit with the view of interaction-based evolution: they demonstrate cooption and emancipation, stabilization and stereotypy, and evolution from fuzzy to sharp. But perhaps most intriguingly, they speak to the arising of novelty in a way that is consistent with network-level evolution.
I will first discuss in detail the example of decoy construction in sand wasps, taken from Evans’s classic ethological work (Evans 1966a, b). Readers who wish to skip this example may continue directly to the final and most important organismal level example to be discussed here—that of egg retrieval by backward walking in the nightjar (Sect. 4.13)—where I will demonstrate all the elements discussed in this paper in one, with an emphasis on the central point of novelty.
To make a nest, the Bembicinae (previously called Nyssoninae) sand wasps dig a tunnel of many body-lengths, at the end of which they build a cell or a complex of cells, where they place their offspring and the prey on which the offspring will feed (Evans 1966b). They have natural enemies—two taxonomic groups of flies (the bee flies, Bombyliidae, and miltogrammine flies, Sarcophagidae) and two taxonomic groups of parasitic wasps (the cuckoo wasps, Chrysididae, and “velvet ants,” Mutillidae)— that parasitize their nests by laying there, and whose larvae either takes up valuable resources or destroy the larvae of the sand wasp. Parasites of the former two groups seek the nests of their hosts by sight, and of the latter two groups by touch and odor—they tap the soil with their antennae while searching for their target (Evans 1966b). Across the sand wasps we find various techniques of hiding and concealment as well as a decoy construction technique (Evans 1966b).
Our example concerns the decoy construction: Some species of sand wasp dig a false burrow (or multiple such burrows) next to the real one and leave it (or them) open, while leaving the real nest burrow closed. Various parasites have been observed to either lay their eggs or linger in the decoys. Evans hypothesized that false burrows originated in a behavior that had a different purpose—that its origin is in cooption—and that the process of the evolution of digging false burrows was a process of improvement through stereotypy, together with emancipation (see also Tsuneki 1963).
He based his hypothesis on the following facts. Very commonly across the Bembicinae, the wasps close the entrance to their nest from the outside before leaving it, either temporarily with a small amount of soil before leaving temporarily for provisioning, or with a large amount of soil at the final closure before leaving for good; and both within and outside of the Bembicinae, species have been observed where individuals obtain soil for nest closure mostly from several or one particular spot/s around the entrance. In this case they leave behind a small pit or pits of a size that depends on how much a particular spot was used. The tendency to take soil from a particular spot or spots appears to relate to environmental conditions, where individuals quarry soil for closure when loose soil is not as easily available (Evans 1966a), though it also has a genetic component (Evans 1966a). The more soil is quarried from a particular spot, the bigger the pit left behind. In Bembecinus neglectus, for example, most individuals took the soil for closure from several particular spots around the entrance, so that a ring of small depressions was left behind. But some took it mostly from one particular spot, which formed a “depression or short “false burrow” up to 1 cm deep” (Evans 1966b, p. 137).
Now, in the genus Bembix, which typifies the advanced behaviors of the Bembicinae, we see species with decided false burrows. Consider three species: Bembix amoena, B. texana and B. sayi. In B. amoena, false burrows are of irregular occurrence and spatial pattern and are relatively short, and the burrowing is still almost always associated with quarrying soil for closure. Most individuals obtain soil for the initial closure by scraping a small amount of soil from each side of the nest entrance, and occasionally from a particular spot or spots, creating short false burrows that stretch in a direction of 90 degrees or a bit less left or right of the direction of the true nest, obliquely into the ground. These short false side burrows varied in length from barely perceptible to 2 cm long, with two exceptional cases observed at 3 and 5 cm long (Evans 1966b). Evans (1966b) noted that, in one population, about half of the nests had no such false side burrows, about a quarter had one, and the rest had two such false side burrows at one time or another. In addition, individuals also collected soil from opposite of the nest entrance, most often, but not always, for the final closure (which requires more soil), which resulted either in a furrow going through the mound of soil opposite the true nest (a mound resulting from the excavation of the true nest), or in a burrow running under that mound obliquely through the ground. The former appeared a considerable number of times, (Evans 1966b, p. 280) and were of varying length, between 1 and 7 cm long. The latter appeared rarely (Evans 1966b), with only three cases noted, at 1.5, 2 and 3 cm long. Evans (1966b, p. 281) noted that two of these were made following final closure in a manner similar to that of Bembix sayi (see below), which seems to suggest that these two rare instances occurred not in the service of obtaining soil for closure.
Besides the burrows themselves, the manner and timing of construction of the burrows was also variable of course (Evans 1966a, b). The burrows on the sides, when they occurred, occurred sometimes along with the initial closure and sometimes along with later closures. The back burrows and furrows, when they appeared, appeared often along with the final closure but sometimes along with earlier closures, and the final closure did not always involve them. While burrows were sometimes revisited and expanded, they were sometimes accidentally filled while making a closure. Likewise, the spatial pattern resulting at the end was variable, with 0 or 1 or 2 side burrows and 0 or 1 back burrow or furrow (Evans 1966a, b). Note that, although the soil was generally taken for closures, parasites were distracted by the false burrows that resulted (Evans 1966a).
In B. texana, construction of false burrows is more or less regular, and the soil is not used for closure. Typically, individuals construct one short but relatively persistent false burrow on each side of the entrance, right after the initial closure is made (Evans 1966b). The method of construction is not yet entirely stereotyped, with some individuals digging one burrow and then the other, and others alternating in digging both (Evans 1966b, p. 325).
In B. sayi, construction is invariable and emancipated: all females dig one strong back burrow 4–22 cm long under the mound after completion of final closure (which also means that the soil is not used for closure) (Evans 1966b, a).
The three species above exemplify certain general trends (Evans 1966b, a). The primitive cases of false burrows, where the burrow is but a small pit, are unreliable and irregular in appearance. The “transitional” case of B. amoena shows burrows appearing in a notable number of cases but still rather irregularly. They are often longer than “small pits” but are still relatively short and vary greatly in length. In the advanced cases, the burrows appear with greater regularity and are substantial. In B. sayi, which makes the longest burrows, the burrows appear invariably in all individuals and at a regular time. There is an association between stereotypy and completeness of the burrow (Evans 1966a, b).
In addition, there is an association between stereotypy and emancipation of burrow-making from its previous cause (Evans 1966b, a). That is, limited quarrying in the service of obtaining soil for closure is a widespread phenomenon, and tends to be irregular in occurrence; whereas, in contrast, regular burrows are the result of burrowing for its own sake, an operation not used for closure, and are constructed at regular times before or after closure, depending on the particular species concerned. In some of the advanced species where burrow-making is thus emancipated, the wasps refresh or fix burrows that have been destroyed (Tsuneki 1963), which further clarifies that they are programmed to maintain a certain pattern of false burrows. The above characteristics are also associated with increased regularity of the spatial pattern of the burrows, with each of the different emancipated species having its own idiosyncratic characteristics of construction (Evans 1966b, a).
Furthermore, not only have emancipated burrows never been observed in species that lack closures, but in addition, a careful examination of the data in Evans (1966b) shows that, even though they are no longer used for closure, emancipated back burrows are temporally associated with final closures, and emancipated side burrows are temporally associated with initial closures, which supports the fact that the origin of emancipated burrows is in closure-making.
Thus, evidence clearly supports the predictions of interaction-based evolution. The evolution of false burrows originated in cooption—in emerging high-level interactions between preevolved elements like digging, quarrying and making closures, and environmental elements like sand conditions. That starting state was one of high variance in behavior and outcome within and between individuals. Evolution then proceeded from fuzzy to sharp: through a process of convergence and gradual stabilization of the trait as a whole toward a stable, emancipated and clock-work-like state. The process was one of improvement together with and at the same time as stereotypy and emancipation. Note that it is not the case that complete but irregular burrows evolved first, and then were stabilized. That is, stereotypy, or uniformity, is not an outcome of a force of stabilizing selection separate from the selection for the adaptation itself. Rather, stabilization and improvement evolve together as two aspects of the same coin—as inherent concomitants of the adaptive evolution of the whole as a whole, as predicted by interaction-based evolution.
The Emergence of Novelty in the Evolution of Egg Retrieval by Backward Walking
I will now discuss the final and most important organismal-level example that puts all of the elements of the theory discussed here together, while emphasizing the central point of the emergence of novelty. This is the example of the evolution of egg retrieval by backward walking in the nightjar (Caprimulgus europaeus) and other species, which applies to eggs that have rolled far outside the nest. Before we can understand it, we must first see what the shifting motion in birds is.
The shifting motion in birds is ancient and involves rolling an egg with the beak until it reaches under the body. The egg may have thus gotten in between other eggs and stirred them, and the egg sides that are pointing up are thus changed (Tinbergen 1960). Shifting may be needed to ensure even temperature distribution to the eggs (Caldwell and Cornwell 1975), and is performed upon arrival at the nest, or when the tactile stimulus provided by the eggs while brooding is not satisfying, or spontaneously after a long spell of quiet brooding (Tinbergen 1960). In terns, the shifting motion will move an egg about 2–3 inches.
Coming back to our case of egg retrieval, in terns (e.g., Onychoprion fuscatus), the general situation is as follows (Watson and Lashley 1915; Tinbergen 1960): If they notice an egg lying several inches outside of the nest, they leave the nest right away to it. However, they have an aversion toward being far from the nest, induced by their brooding state, and as they move away from the nest, they slow down, sometimes turning around and returning to the nest without having reached the external egg. But sometimes they do get to the egg, stopping short of it just close enough that they can reach it with the beak and apply the shifting motion to it, which rolls the egg until it is under the breast.
As they shift the egg, they sit down on it to incubate it, but only for a short time (indeed they may at this point be dissatisfied with the tactile stimulus and/or with being outside of the nest). The moment they notice the nest again they stand up and walk to it. In the process, the egg has moved about 2–3 inches toward the nest due to the shifting motion.
Having returned to the nest and started brooding the eggs there, they soon notice the external egg again, venture out toward it again, and repeat the process, and the egg moves 2–3 inches again toward the nest. Thus, after several trips, the egg finds its way back to the nest.
The behavior that results in the egg being moved back to the nest is clearly unstructured. The brooding of the external egg outside of the nest and the back-and-forth trips show lack of insight or “analysis of the situation as a whole” (Watson and Lashley 1915, p. 83), as the different actions taken in the situation are under the proximate control of different preevolved instincts. In accordance with Tinbergen (1960), these instincts are competing with each other for expression: the desire not to leave the nest, the desire to return to the nest, the desire to brood eggs, and the desire and ability to shift an egg. Also, as Marshall noted for the common tern (Sterna hirundo) (Marshall 1943), there is much variance in the behavior and its outcome, with eggs sometimes being rolled back into the nest and sometimes not, and this variance is thought to reflect both individual variance and situational factors (Marshall 1943).
In other birds, however, such as greylag geese (Anser anser), black-headed gulls (Chroicocephalus ridibundus) and nightjars, the bird walks straight up to the egg, puts the beak over it as it would in shifting, but instead of incubating the egg there, it then walks backwards all the way to the nest in one shot while shifting and dragging the egg under its beak (Kirkman 1937; Tinbergen 1960).
According to Tinbergen, this egg rolling observed in nightjars and other birds evolved from shifting and other elements of the situation (Tinbergen 1960). Indeed, the fact that the birds are using a shifting motion while walking backward (even though rolling with the wing would have been much more efficient) together with the fact that shifting is ancient, supports this hypothesis (Tinbergen 1960). In fact, Tinbergen notes that the very controversy about whether egg retrieval is an independent adaptation or a by-product of a confluence of instincts in different species shows its route of evolution (Tinbergen 1960).
The argument that this backward walking behavior appearing in nightjars and other birds evolved from a situation akin to that of the terns exemplifies several elements of interaction-based evolution in one: The trait has evolved from fuzzy to sharp; from unstructured and inefficient to structured and efficient; from variable and unstable to stable, stereotyped and “rigorous.” In addition, we also see emancipation in it: the return back to the nest originally required the visual stimulus of seeing the nest, but now is triggered automatically as soon as the shifting motion begins and requires no turning-around to the nest. We also see fusion: the going-to-the-egg and the coming-back-to-the-nest legs have been fused together in one sequence unleashed by the stimulus of seeing the external egg for the first time, whereas previously they were two separate legs each triggered by its own visual stimulus. The whole situation has been simplified, the path has been straightened up. In fact, the simplification has been the creation of a method from a previously non-methodical occurrence, when all the while the whole evolved as a whole, not by the addition of independent elements one at a time.
On top of all of the above, one topic deserves a special emphasis: novelty. The example of egg rolling shows clearly that different instincts or elements have the inherent ability to come together into new, useful interactions that together can achieve what had been unachievable before by any one of those instincts alone. Twice we see that this coming together of pre-evolved elements into useful, high-level interactions breaks a barrier in terms of being able to do something that could not have been done before. First, the confluence of instincts for shifting, brooding and returning to the nest effectively allows the egg to be returned to the nest after several trips, even if in a haphazard way, when none of these instincts by itself is capable of achieving this, nor did any of them originate due to pressure for such egg retrieval. The second barrier broken was this: the invention of backward walking while shifting allows retrieval of the egg in time that is proportional simply to the distance to the egg, whereas the haphazard way only allows retrieval in time that is quadratic in distance. This improvement allows nightjars to retrieve eggs from many yards away, which would not have been effectively possible in the case of terns (indeed terns retrieve eggs from only several inches away). Thus, emancipation and fusion have created a behavior that now applies to a broader range of situations than the ancestral traits applied to. Indeed, some of these birds now dwell in beaches where eggs can indeed be blown away by wind a great distance.
These breakings of barriers exemplify novelty. The source of the novelty is the inherent ability of elements to come together into new and useful high-level interactions. These elements come together first in a haphazard state. Their complex interaction then serves as a substrate for simplification under performance pressure, where new such elements will be formed. I propose that this cycle is the heart of the evolutionary process; and that it is simplification under performance pressure that is responsible for this inherent usefulness of elements—for their propensity to come together into new, useful interactions that they have not been directly selected for.
While consistent with previous works on the evolution of novelty, as will be discussed in Sect. 4.16, this point provides an understanding of novelty in evolution that is completely different from and not reducible to the traditional notion of accidental mutation and natural selection. The novelty that drives evolution here arises from the coming together of high-level “modules,” i.e., from the network as a whole. It is not a local, “misspelling”-like change at the genetic level. This demonstrates the key point that the source of invention in evolution does not need to be accidental mutation. Instead, I argue that non-accidental mutation and natural selection together process information gradually, and the source of novelty in evolution is the resulting inherent ability of elements to come together in useful high-level interactions, an ability due to simplification under performance pressure.
Watson and Lashley (1915) saw that the outcome of the haphazard mode of egg retrieval was not intentional. They noted that the egg rolls in the direction of the nest simply because the bird is oriented directly away from the nest as it reaches the egg, so that the shifting motion happens to bring the egg a bit closer to the nest each time. From this they concluded that the egg finds its way to the nest by lucky happenstance. But this lucky happenstance is a far cry from the traditional notion of novelty in random mutation. First, it is not a local accidental mutation that invents, but rather the process starts with high-level interactions, and gradual network evolution creates a new trait from this source. Second, a deep new question arises. Should we call this source of novelty “randomness” or “lucky happenstance” at the phenotypic level, and say no more? There is logic to the present situation that goes beyond the purely coincidental. That is, although the egg rolls to the nest only because of the bird’s orientation, it is oriented in this way because it is walking straight up to the egg from the nest. Each action—walking straight up, shifting and returning—is efficient and elegant, and together they create a situation that, while haphazard, is not purely random, but can be seen as a fuzzy sort of “shifting in an extended nest.” Thus, a confluence of instincts, each useful in and of itself, together give rise to something useful that is different from each of them, but which at first can only appear in a roundabout, highly variable, even though not purely accidental, fashion. As such, it serves as material for evolutionary simplification and streamlining, which ends up creating something that can be useful in contexts that go beyond the one that originated it.
It is intriguing that an unqualified notion of the accidental does not sufficiently explain novelty here. When we apply this way of thinking to other cases of cooption, we will see that, individually, they may appear more or less accidental than the above case; but they are not, in general, “pure coincidences.” This, together with the question of how exactly simplification under performance pressure leads to inherently useful elements, contributes a new dimension to the science of novelty (Gould and Vrba 1982; Müller 1990; Müller and Wagner 1991; Gould 2002; Moczek 2008; Wagner 2014).
While others have discussed the possibility of cooption being a source of novelty (Gould and Vrba 1982; Hallgrímsson et al. 2012; Müller 1990; Müller and Wagner 1991; Schlichting and Pigliucci 1998; West-Eberhard 2003; Müller and Newman 2005; Moczek 2008; Peterson and Müller 2013), this possibility has not been sufficiently distinguished from the view of accidental mutation—cooption has often been treated as an accidental event and another source of novelty in addition to accidental mutation (Williams 1966; Gould and Vrba 1982; Gould 2002). In contrast, interaction-based evolution argues that cooption is neither an accidental event nor another source of novelty in addition to accidental mutation. Rather, the joint action of non-accidental mutation and natural selection gradually paves the way to both genetic and phenotypic cooption through network-level evolution. Thus, neither mutation nor cooption are random in the traditional sense even though they produce surprising things, and they are not separate sources of novelty but come together as two inseparable aspects of one process. In other words, cooption is at the heart of the process of interaction-based evolution and is built into this process.
Thus, while in the traditional view, new genetic information arises by accident at a specific point in space and time, according to interaction-based evolution, novelty is an outcome that arises over time at the network level from the coevolutionary change of many elements. While the drivers of these local changes are not random, these changes still interact with each other globally in a surprising way. Surprise, or novelty, exists, but it is not a mere direct effect of dice rolling.
It is noteworthy that the tern situation is based on conflict, or competition between tendencies. The bird, on the one hand, acts as though it wants to reach up to the egg and incubate it, but on the other hand as though it wants to remain in the nest. It is also noteworthy that there is individual variation in the overall behavior, and indeed, there may be different ways of increasing the probability of success. One way may be to approach the egg without hesitation. Another may be to get back to the nest without delay once the egg has been shifted. There is an inherent conflict in the situation. Both tendencies have something to contribute, but they are conflicting. To strengthen one at the expense of the other may be harmful. One may suppose that evolution needs to take a modest though complex step: to find a solution for returning to the nest immediately and only after reaching the egg while engaging it with the beak. This can be achieved, for example, by overcoming the tendency to incubate but only while standing outside of the nest. The relevant rule to evolve, “incubate in the presence of eggs AND when standing in the nest” is simple but non-linear. In performing this evolutionary step, the convergence process described by Livnat (2013) may lead to the crystallization of the commonality between successful individuals while resolving the conflict inherent in the situation, making evolution a process of conflict resolution.
The example also shows us, of course, that the whole is greater than the sum of its parts and that the organism evolves as a whole. Conceptualizing evolution in this way provides an answer to the many inconsistencies that arise from the accidental mutation framework and the related conceptualization of evolution as a one-step-at-a-time type of process, such as the fact that the latter often lead us to surmise difficult evolutionary transitions leading to complex adaptations where the intervening steps are not adaptive in and of themselves (Wright 1931, 1932; see also Moczek 2008; Hallgrímsson et al. 2012; Arnold 2003; Müller and Newman 2005; Peterson and Müller 2013; Kaji et al. 2016).
Finally, a connection similar to the one pointed out between punctualism and gradualism in morphological evolution (Müller and Streicher 1989; Müller and Wagner 1991; Moczek 2008; Hallgrímsson et al. 2012; Peterson and Müller 2013) can be seen in the above behavioral example. Suppose that, as the underlying instincts evolve and are being emancipated and adjusted, the balance of tendencies gradually changes such that the tendency to incubate the external egg while outside of the nest falls below the tendency to return to the nest, while the tendency to return remains balanced with shifting, so that returning and shifting are expressed together. In that case, these tendencies may evolve gradually, while the new trait may arise punctually: it may be possible for a bird species to evolve backward-walking retrieval as a whole and rather rapidly, causing an evolutionary “phase transition” at the level of the observed behavior. Backward walking will then appear first in one individual, then in another, then more and more—it will arrive “like the rain.” Thus, punctualism is better understood when we start thinking of it in terms of network evolution, as an outcome of gradual network-change trends that interact with each other (Müller and Wagner 1991; Moczek 2008; Hallgrímsson et al. 2012; Peterson and Müller 2013).
How Evolution Learns: Circuitous Versus Accelerated Development
The example of the evolution of egg retrieval highlights a fifth aspect of innateness. The terns are not learning to retrieve the egg, yet their haphazard emergent behavior which results in egg retrieval does not seem to fit the term “innate.” There is another aspect to innateness, and that is the degree to which a behavior develops straightforwardly and quickly in an endogenously driven fashion. For example, though an emerged butterfly takes to the air after it finishes preparations (like drying up its wings), this behavior of taking off is not actually driven but only triggered by finishing preparations, and is otherwise endogenously driven. In contrast, the behavior which results in egg retrieval in the terns arises circuitously and at a high level, from a meeting of different inborn behavioral elements as well as environmental factors which play a more inherent role in inducing the behavior: the visual stimuli and conflicting instincts do cause the retrieval of the egg. This high level meeting of modules, both internal and external, now serves as the source of evolution from fuzzy to sharp, at the end of which a new innate module, consisting of a combination of the previously independent elements, will arise (that of backward walking). This aspect, namely, how quickly, straightforwardly and endogenously a behavior (or a trait in general, including morphological traits) arises in development is important for evolutionary acceleration: In the initial circuity there is a potential for “straightening up,” there is a potential for simplification that will lead to the further breaking of barriers (e.g., substantially faster egg retrieval). The environmental factors play a more inherent role in inducing the behavioral outcome in the tern situation than in the butterfly situation, which means that, in becoming emancipated from them in the course of evolution, the life form is “learning” from the environment evolutionarily. That is, it now produces more endogenously what the environment helped to produce before. I argue that this emancipation is the intergenerational “learning” that is done by evolution, drawing an analogy between evolution and learning (see more in Sect. 5.7).
It is interesting that those who have tried to define innateness often seemed to mean that, in contrast with learned behavior, innate behavior is in a sense “predetermined” (Papaj 1993). In other words, in innate traits, the fit with the environment is predetermined, as opposed to learned behavior or morphological plasticity, where the fit is “acquired.” However, notice that this predetermined fit is adaptation. In a system-first view of evolution, the evolution of innateness, or automatization, is the evolution of adaptation. And, according to interaction-based evolution, the evolution of adaptation involves network-level evolution and the acquisition of a new phenotypic meaning as a result of the changing context in which modules are embedded.
The Engine of Evolution
Interaction-based evolution argues that the process whereby a population converges on an adaptation (Livnat 2013; Sects. 4.10, 4.12, 4.13) is a process that converts information from a less orderly to a more orderly state. It proceeds from a fuzzy to a sharp, well-working and stereotyped state. However, evolution is not only a fuzzy-to-sharp process, in that the fuzzy source must first arise. The progress from fuzzy to sharp is therefore only a half of a cycle of the “engine of creativity” that is evolution. The other half is that previously made sharp elements come together at a high level to make the new fuzzy source (e.g., the different instincts in the tern situation come together into a disorderly form of egg-retrieval), from which new sharp elements can be made (e.g., backward walking).Footnote 26 I argued that simplification under performance pressure connects the two parts of the cycle. The simple elements it creates not only are improvements but also come together in new complex interactions which serve as the raw material for the next round of simplification. Thus, novelty arises not from accident, but from evolutionary work.
How Interaction-Based Evolution Contributes to Past Literature on the Evolution of Novelty
We can now see how interaction-based evolution confirms previous, pioneering literature on the evolution of novelty. Even though the latter focused on the evolution of morphology (Müller and Wagner 1991; Moczek 2008; Wagner and Lynch 2010; Peterson and Müller 2013), whereas the observations above pertain to the evolution of behavior, both conclude that network-level evolution is key to the evolution of novelty, and furthermore agree on multiple fundamental points that follow from this: First, cooption is central to novelty, as are elements of network evolution like duplication, fusion etc. (Gould and Vrba 1982; Müller 1990; Müller and Wagner 1991; Schlichting and Pigliucci 1998; West-Eberhard 2003; Hallgrímsson et al. 2005; Müller 2007a; Hallgrímsson et al. 2012; Wagner 2014; Lynch et al. 2015). The emergence of a “byproduct,” where a trait evolved for one purpose comes to serve another, is not a side-issue but absolutely central to evolution (Sects. 2.2, 3.4, 4.5, 4.12, 4.13, 4.15; Müller 1990; Müller and Wagner 1991; Müller and Newman 2005; Moczek 2008; Peterson and Müller 2013). Second, cooption is needed for the otherwise inexplicable incipient stage of a novel, complex adaptationFootnote 27 (Moczek 2008; Hallgrímsson et al. 2012; Arnold 2003; Müller and Newman 2005; Peterson and Müller 2013; Kaji et al. 2016). Third, the common distinction in the literature on novelty between two stages of evolution—the modification of an existing character and the formation of a new character (Gould and Vrba 1982; Müller and Wagner 1991; Müller and Newman 2005; Wagner and Lynch 2010; Hallgrímsson et al. 2012)—corresponds to the two stages of the evolutionary cycle discussed here (see Sect. 4.15). Fourth, network-level evolution—the evolution of a complex whole—allows for the conversion of gradual to punctual change via the passing of thresholds (we have seen this in the egg retrieval discussion, Sect. 4.13; Waddington 1957; Müller and Streicher 1989; Müller and Wagner 1991; Moczek 2008; Hallgrímsson et al. 2012; Peterson and Müller 2013).
At the same time, interaction-based evolution also contributes to this literature. First, as mentioned, while the latter focused on morphology, in the above I have provided complementary examples from the evolution of behavior. Second, even though past literature has recognized the centrality of cooption for novelty and identified phenomena that facilitate cooption, such as gene duplication, “weak regulatory linkage” and more (Ohno 1970; Kirschner and Gerhart 2006; Gerhart and Kirschner 2007; Lynch 2007), it has not considered the possibility that there is a fundamental reason underlying the inherent ability of biological entities to be coopted, or that this reason connects to non-accidental mutation. This paper has proposed that simplification under performance pressure actively generates cooptability (see Sect. 3.4). Furthermore, it has proposed that simplification under performance pressure connects to non-accidental mutation as will be summarized in Sect. 5.2. Third, while this paper agrees with past literature on the distinction between the two stages abovementioned, it does not assume that the modification of existing characters can be accounted for by the traditional view of adaptation based on accidental mutation and natural selection, and that only the arising of a novel character cannot. Instead, it argues that the mutations that underlie network-level evolution throughout both stages are non-accidental and enable simplification under performance pressure; that this simplification under performance pressure is what makes a character cooptable while modifying it; and that the two stages thus come together in one unified process: one stage actively leads to the other.
Thus, the present paper bears on a major gap in traditional evolutionary theory. Multiple authors (Gould and Vrba 1982; Hallgrímsson et al. 2012; Müller 1990; Müller and Wagner 1991; Schlichting and Pigliucci 1998; West-Eberhard 2003; Müller and Newman 2005; Moczek 2008; Peterson and Müller 2013; Lynch et al. 2011) have recognized the importance of cooption at both the molecular and organismal levels. Graur and Li called it “the paradigm of molecular evolution” (Graur and Li 2000, p. 304). However, traditional population genetics focused on trying to explain the accumulation of slightly beneficial changes toward improvement in the same adaptation, not on how an element evolved for one purpose can later become useful for another (Gould and Vrba 1982; Müller and Newman 2005; Wagner and Lynch 2010). This paper proposed that there is an active reason underlying cooptability—simplification under performance pressure—and that this active process offers an alternative explanation to many biological phenomena at both the genetic and phenotypic levels besides economical considerations under accidental mutation and natural selection.