Phylogeography of Seaweeds in the South East Pacific: Complex Evolutionary Processes Along a Latitudinal Gradient
The coast along the temperate South East Pacific (SEP) presents a simple linear topography with a north-south orientation spanning more than 4600 km. However, environmental heterogeneity associated with two major biogeographic boundaries has been described along the SEP (30–33°S and 42°S). Recent phylogeographic studies of seaweeds revealed the existence of different cryptic species along the SEP coast and that most of the genetic breaks between them are broadly congruent with the biogeographic boundaries. These phylogeographic patterns characterized by genetic discontinuities could be attributed to historical vicariance or to budding speciation. For SEP seaweeds, two major phylogeographic patterns are observed. Endemic species living north of 42°S show complex haplotype networks and an almost complete genetic isolation between populations located only a few kilometres from each other. This extreme genetic patchiness has been related to the combined effects of limited dispersal, reduced population size and high population turnover of these intertidal seaweeds due to stochastic effects of climatic and tectonic catastrophes. On the other hand, species with a range distribution limited to the south of 42°S and inhabiting the area highly affected by the coastal ice cap during the Last Glacial Maximum (LGM), show typical signatures of post-glacial demographic expansion. Finally, molecular studies reveal that several species are recent immigrants from New Zealand, demonstrating the importance of oceanic dispersal in shaping the diversity of the SEP.
KeywordsBiogeographic boundaries Budding speciation Chile Cryptic species Phylogeographic breaks Post-glacial recolonization
The temperate South East Pacific (SEP) represents one of the most productive marine ecosystems of the world. Research interest in this region has increased during the recent years and consequently, phylogeographic studies have started to accumulate at a rapidly increasing rate. Areas of research range from simple exploratory analyses of genetic variation focusing on the identification of genetic resources, to specific assessments of the role of biogeographic discontinuities in the evolutionary history of an organism. Most studies are based on a ‘single marker-single species’ sampling design and focus on different areas of the SEP which have limited the description of general genetic trends in the region. Indeed, some studies reveal strong genetic structure and have stated that highly regionalized historical and contemporary factors are driving these patterns (see, for example Tellier et al. 2009; Fraser et al. 2010a; Brante et al. 2012; Montecinos et al. 2012; Varela and Haye 2012), whereas other studies suggest that species form single genetic units that share a common demographic history (for examples see Cárdenas et al. 2009; Haye et al. 2010, 2012). Recently, the first multispecies comparative study was conducted in central and northern Chile to investigate the role of oceanographic and biogeographic boundaries present around 30°S (Haye et al. 2014). This study suggests that genetic structure among populations in eight marine invertebrate species can be largely explained by dispersal potential and historical processes that limit gene flow near 30°S (Haye et al. 2014). Indeed, species with short pelagic larval duration display a clear-cut phylogeographic discontinuity coincident with the biogeographic transition zone at 30°S whereas the species with long-term pelagic stage do not show a genetic discontinuity. Another biogeographic boundary described at 42°S (Camus 2001) was also reported to match the location of genetic discontinuities (i.e. cryptic species were defined on the both sides of the 42°S; Fraser et al. 2009). Along the SEP, the concordance between biogeographical boundaries and genetic breaks has been attributed to historical vicariance caused by oceanographic or climatic features (Tellier et al. 2009; Zakas et al. 2009; Brante et al. 2012; Montecinos et al. 2012; Varela and Haye 2012; Haye and Muñoz-Herrera 2013; Haye et al. 2014).
The use of molecular markers has allowed for the identification of many cryptic species in marine organisms. Molecular identification has been especially useful for studying organisms, such as seaweeds, that display few diagnostic characters and are morphologically simple (Leliaert et al. 2014). The lack of morphological characteristics that differ between evolutionary units (i.e. species as defined by the lineage species concept) has for some time obscured the study of biogeographic boundaries, species distributions, and speciation processes in seaweeds. For example, in a molecular study of the red alga Portieria hornemannii in the Philippine archipelago, Payo et al. (2013) demonstrates that this unique morphospecies is in fact composed of 21 cryptic taxa. These remarkable findings led to the complete reinterpretation of Portieria’sbiogeography in the region. Even if many cryptic species have been reported in marine algae along the SEP, the general processes that contribute to speciation and genetic breaks, and how these relate to biogeographic boundaries and vicariance, have not yet been investigated for these organisms.
In this chapter, we intend to discuss new findings of seaweed phylogeographic structure and cryptic sister species distributions along the SEP to gain some biogeographic insight and to identify some of the major drivers of evolutionary processes that have affected Chilean seaweeds.
10.2 Major Biogeographical Characteristics of the SEP Coast: Linear Gradient or Strong Regional Pattern?
Based partly on these contrasting topological and oceanic characteristics, several studies have proposed the existence of two main biogeographic provinces along the SEP: the Peruvian and Magellan provinces (Camus 2001; Thiel et al. 2007, and references therein; Fig. 10.1a). The Peruvian province is characterized by the presence of a strong tropical component in both its flora and fauna while there is a predominance of species of subantarctic origin in the Magellan province. An Intermediate Area that combines mixed components of the two neighbouring provinces extends from 30–33°S to 42°S (Camus 2001; Thiel et al. 2007). The southern limit of the Peruvian province at 30–33°S is considered to be a major transition zone in the oceanographic features, with strong but seasonal upwelling south of this limit and weak but persistent upwelling conditions in the north (Broitman et al. 2001; Thiel et al. 2007; Tapia et al. 2014). Fenberg et al. (2015) have shown that upwelling-related variables are the best overall predictors of biogeographic structure of northeast Pacific rocky intertidal species, and upwelling seems to be especially influential on assemblages of algae and invertebrates with low-to-medium dispersal capabilities. In this context, it is interesting to note that spatial heterogeneity in the upwelling regime seems to be a major determinant of biogeographic boundaries in the SEP. A second major habitat discontinuity at 42°S, linked with differences in topography, freshwater input, and current dynamics, determines the northern limit for the Magellan province (Brattström and Johanssen 1983; Fernández et al. 2000; Camus 2001; Thiel et al. 2007) (Fig. 10.1a).
The SEP biogeographic boundaries are well correlated with present-day oceanographic conditions but these have not been fully persistent throughout evolutionary history (Fig. 10.1b). However, despite climatic and oceanographic fluctuations, the regions of both 30–33°S and 42°S also represented major habitat discontinuities in the past. First, the northernmost limit of the coastal ice sheet during the Last Glacial Maximum (LGM, 0.026–0.019 Ma) was established near 42°S (McCulloch et al. 2000; Fig. 10.1b). It is well accepted that no coastal ice formed north of that latitude, where potential refugia are proposed for cold-water species. Models of ice sheet extension propose that the southernmost tip of South America, near Cape Horn, was also free of coastal ice and provided the second glacial refugium for marine species of the Magellan province (Hulton et al. 1994, 2002). Indeed, many seaweeds are endemic to the Strait of Magellan, the Beagle Channel, and the Cape Horn archipelago (53–55°S) and are completely absent from the rest of the Magellan province (reviewed by Fernández et al. 2000; Santelices and Meneses 2000). Second, the Intermediate Area experienced historical changes in habitat quality. During glacial periods, the influence of the ACC shifted towards the north leading to a northward shift of the Humboldt/Cape Horn current split (Fig. 10.1b). This change in oceanic circulation likely caused a strong reduction in upwelling in the Intermediate Area, as shown by a reduction of plankton deposits in the region associated with the LGM (Mohtadi and Hebbeln 2004; Kaiser et al. 2005; Verleye and Louwye 2010). In contrast, the area north of 30–33°S is considered to be an area with long-term persistence of upwelling (Mohtadi and Hebbeln 2004).
In addition to the historical geographic and climatic barriers in this region, short-term environmental disturbances have also been taken place repeatedly throughout the SEP’s history. Two major factors have been shown to cause such disturbances. First, the El Niño–Southern Oscillation (ENSO) events that consist of a 2–7 years alternation of a cold period (La Niña) and a warm period (El Niño) (Tarazona and Arnzt 2001). ENSO fluctuations began during the Holocene (Moy et al. 2002) and have intensified during the last 5000–3000 years. El Niño events produce strong mortality in seaweeds due to abrupt increases in the temperature of coastal waters and decreases in nutrient concentrations along the northern part of the SEP, from 6°S to ~30°S (Camus 1990; Martínez et al. 2003). Second, tectonic activity also causes strong seaweed mortality along the extensive coastline of the SEP. Specifically, the sudden coastal up-lifts and downward drops of several meters during major earthquakes, accompanied by major tsunamis, are detrimental to coastal seaweeds (Darwin 1839; Castilla 1988; Castilla et al. 2010; Jaramillo et al. 2012). Several of these coastal up-lifting events have been reported in recent decades and their effects on intertidal communities have been well described (Castilla 1988; Castilla et al. 2010; Jaramillo et al. 2012; Fuentes and Brante 2014; Hernández-Miranda et al. 2014; Ortega et al. 2014).
10.3 Phylogeography: The Problem of Cryptic Species and Consequences for the Delineation of Species Range Distributions
The SEP region hosts nearly 600 seaweed morphospecies of which about 27 % are endemic (Meneses and Santelices 2000). While global diversity gradients for a wide range of taxa follow a classic latitudinal pattern, characterized by a decrease in richness from the tropics to the poles, seaweed morphospecies richness tends to increase with latitude along the SEP (Santelices 1980; Santelices and Marquet 1998; Ramírez 2010; Keith et al. 2014). This inverted latitudinal seaweed diversity pattern, which exists worldwide (Kerswell 2006), was recognized recently by Keith et al. (2014) as a potential consequence of niche conservatism (Pyron and Burbrink 2009). Indeed, contrary to the majority of taxa, macroalgae originating in temperate zones and may have been limited in their ability to colonize tropical regions due to competition with established corals and predation by herbivores (Keith et al. 2014). Along the SEP, the high diversity of seaweeds at high latitudes has been linked to the presence of a highly diverse subantarctic flora with a range distribution that is restricted to the tip of South America (Santelices 1980; Santelices and Marquet 1998; Ramírez 2010). Based on clustering of the flora, Santelices (1980) distinguished three distinct areas along the coastline: the tropical area of northern Peru (4–5°S), a broad intermediate area (5°–53°S) and the southern tip of South America (53–55°S). Within the broad intermediate area, both brown and red seaweeds show clear biogeographical breaks at 30–33°S and 42–43°S (Meneses and Santelices 2000). The dominance of endemic species diminishes southward as they are replaced by subantarctic species, which are distributed in the cold waters of the South Pacific and the Southern Ocean (Santelices 1980).
Species richness along the SEP has probably been underestimated in the above cited studies as species determination was based solely on the use of morphological characters. The development of molecular genetic tools over the past two decades has strongly demonstrated our inability to correctly identify species on the basis of morphological characters alone. Using molecular markers, the presence of cryptic species has been revealed in many taxonomic groups and in various habitats (e.g. in marine environments Knowlton 1993, 2000; and in particular, in algae, see the recent review Leliaert et al. 2014). Studies based on molecular markers have accumulated compelling evidence that algal names have been applied incorrectly and morphological identification could lead to erroneous conclusions about trait evolution in seaweeds (see, for example the comparative analysis of chemical defence in Gracilariaceae, Weinberger et al. 2010). These erroneous taxonomic assignments have also revealed that seaweeds could have higher species diversity, and species could be more regionally confined than previously thought (see for example Tronholm et al. 2012; Payo et al. 2013; Pardo et al. 2014; Vieira et al. 2014).
Although the sample sites, sample sizes and level of diversity differ among taxa (Table 10.1), two major phylogeographic structuring patterns can be observed (Fig. 10.2). While endemic species living north of 42°S show complex reticulated haplotype networks, species that have recently colonized the SEP or endemic species with a range distribution limited to the south of 42°S generally show simple star-like haplotype networks (Fig. 10.2). Because these differences reflect distinct evolutionary trajectories and demographic histories, in the following sections, we discuss the historical and contemporary scenarios that likely shaped these different patterns of phylogeographic structure.
10.4 Parapatric Distribution and Speciation Processes Along a Linear Coast
10.4.1 Cryptic Phylogenetic Species Within Previously Reported Morphospecies: Phylogenetic Breaks that Do not Always Fit the Biogeographical Boundaries
The endemic red alga M. laminarioides dominates the middle-high intertidal rocky shore while the kelps L. nigrescens and D. antarctica are found in wave-swept low intertidal areas. Both M. laminarioides and L. nigrescens morphospecies, considered poor dispersers (Santelices 1990), show genetic differentiation at short geographic distances (hundreds of meters to a few kilometres, Faugeron et al. 2001, 2005; Tellier et al. 2011a). Conversely, the bull kelp D. antarctica, characterized by a buoyant thallus is considered to be a good disperser through rafting (Fraser et al. 2009, 2010a, b; also see chapters by Macaya et al. 2016 and Fraser 2016 in this volume).
Despite ecological differences among these morphospecies, molecular studies have revealed that each is subdivided into phylogenetic species, i.e. reciprocally monophyletic and highly divergent clades (see Fig. 10.3). Two clades were recovered for L. nigrescens (Tellier et al. 2009), whereas three clades were recovered for M. laminarioides (Montecinos et al. 2012). D. antarctica is a species complex of four deeply divergent taxa, of which only two are present along the SEP coast (i.e. “central Chile” and “subantarctic”, Fraser et al. 2010a, b).Within each morphospecies, molecular markers were congruent in revealing the occurrence of cryptic species distributed in parapatry along the SEP coast (Figs. 10.2 and 10.3). The location of phylogeographic discontinuities are specific to each morphospecies: 30°S for L. nigrescens, 33°S and 38°S for M. laminarioides, and in-between 44°S and 49°S for D. antarctica. Interestingly, speciation processes seem to be tightly linked to the processes driving the biogeographic discontinuities. In L. nigrescens and D. antarctica and between M. laminarioides “north” and “center” lineages, genetic discontinuities broadly match the biogeographic boundaries (Meneses and Santelices 2000; Camus 2001; Thiel et al. 2007), which is also the case for several invertebrate species (Brante et al. 2012 Varela and Haye 2012; Haye et al. 2014). However, the genetic break between M. laminarioides “center” and “south” lineages is located between 37°S and 39°S, a region where neither a biogeographic boundary nor a phylogeographic break has been described. The absence of a precise estimate of mutation rates makes it difficult to use molecular clocks to assess the time of divergence among lineages of seaweeds. An exploratory estimation of the historical events at the origin of the divergence among lineages has however been attempted. The separation between M. laminarioides “north” and “center” and between M. laminarioides “center” and “south” were estimated to be between 1.0 and 12.1 Myr and between 0.5 and 5.8 Myr, respectively (Montecinos et al. 2012). The separation between the cryptic species of L. nigrescens (i.e. L.berteroana and L. spicata; González et al. 2012) is estimated to have occurred more recently, between 0.2 and 1.7 Myr (Tellier et al. 2009) and 2.0 and 3.1 Myr (Martin and Zuccarello 2012) depending on the method of estimation. Within D. antarctica, most of the genetic diversity is found around New Zealand where a late Miocene/Pliocene radiation occurred between 1.3 and 9.7 Myr (Fraser et al. 2010b). Even if substantial uncertainty is associated with the timing of lineage splits in the three study cases, the authors agree that they predate Pleistocene glaciations. Because the location and putative timing of the phylogeographic breaks are not fully congruent between taxa, it is not possible to identify specific historical events that may have driven speciation in these intertidal seaweeds (Avise et al. 1987).
In the case of D. antarctica, phylogenetic reconstruction indicates an ancient split of the “central Chile” lineage (Fraser et al. 2009, 2010b) that could have occurred after the first transoceanic dispersal event of the algae from New Zealand, where the genus originates. This allopatric divergence took place well before the diversification of New Zealand taxa from which evolved the “subantarctic” lineage present in Chile (Fraser et al. 2010b). The presence of the “subantarctic” lineage in Chile has been explained by recent, post-glacial transoceanic dispersal from New Zealand and colonization of Patagonia soon after melting of the coastal ice sheet (Fraser et al. 2009, 2010a, b). Therefore, in the case of D. antarctica, the genetic break observed in the SEP around 44–49°S results from a secondary contact between two lineages that have diverged in allopatry on either side of the Pacific Ocean.
Conversely, allopatric speciation has not been proposed as the cause of lineage splitting in either M. laminarioides or L. nigrescens. The genus Lessonia is distributed throughout both New Zealand and Chile, but studies have clearly indicated that divergence between L. spicata and L.berteroana occurred in Chile (Tellier et al. 2009; Martin and Zuccarello 2012). A similar situation has been suggested for M. laminarioides, which is endemic to Chile. While incomplete lineage sorting due to the presence of ancestral haplotypes has been revealed using slow evolving molecular markers, reciprocal monophyly has been systematically observed using faster evolving markers for cryptic lineages of M. laminarioides and for both L. berteroana and L. spicata (Fig. 10.3). The topology of phylogenetic trees built from slow evolving markers was similar for both Mazzaella and Lessonia, with monophyletic derived lineages embedded within a basal polytomy formed by the more ancestral haplotypes (Fig. 10.3). These slow evolving marker tree topologies have been described as a typical signature of budding/peripatric speciation rather than vicariant speciation (Funk and Omland 2003; Crawford 2010). For both the lineage splitting within M. laminarioides and the divergence between L.berteroana and L. spicata, authors have suggested the existence of budding speciation with a sudden expansion at the range limit of the ancestral lineages (Tellier et al. 2009; Montecinos et al. 2012). However, there is a difference in the direction of the range expansion of these ancestral lineages. A range expansion of L. spicata in the area located north of the 30°S could be at the origin of L. berteroana. In contrast, range expansion of M. laminarioides “north” in the area located south of the 33°S could be at the origin of M. laminarioides “center” and “south” (Fig. 10.3; see Tellier et al. 2009; Montecinos et al. 2012 for more details).
Budding speciation (also known as peripatric speciation) was first defined by Mayr (1954) as a speciation process by which an initially small colonizing population becomes reproductively isolated from a species with a larger range. In a paper entitled “Rethinking classic examples of recent speciation in plants”, Gottlieb (2004) developed the argument that this process of speciation in which species ‘bud off’ from ancestral species via small, locally isolated peripheral populations is probably common in plants. In addition, Gottlieb (2004) highlights that recently diverged sister species, for which the overall genetic distance is minimal and the direction of evolution is clear are particularly relevant cases to study this mode of speciation. Many authors have thus argued that budding speciation has a unique signature that, early in the speciation process, sister species should have overlapping or adjacent ranges with very different sizes (i.e. asymmetric ranges) and different realized niche breadths (Funk and Omland 2003; Gottlieb 2004; Grossenbacher et al. 2014; Anacker and Strauss 2014). The prediction of a greater range asymmetry between younger versus older sister pairs was verified recently in two large-scale analyses in plants (114 species of Mimulus sampled in North America, Grossenbacher et al. 2014; 71 sister species from 12 families sampled in the California Floristic Province, Anacker and Strauss 2014). Supporting a scenario of budding speciation, strong ecological niche differences were observed between L. berteroana and L. spicata, including temperature responses (Oppliger et al. 2011, 2012; Vieira et al. 2015), tolerance to air exposure (López-Cristoffanini et al. 2013) and differences in phlorotannin pigments and chlorophyll a fluorescence of PSII (Koch et al. 2015). Niche preferences have yet to be studied for the three lineages of M. laminarioides. The comparison of range sizes of derived and ancestral cryptic species does not seem to fit the prediction of range asymmetry for sister lineages and crypticspecies along the SEP. Indeed, L.berteroana and L. spicata have a very similar range size of about 1500 km which overlaps less than 200 km between 29°S and 30°S (Tellier et al. 2009, 2011a) (Table 10.1; Figs. 10.2 and 10.3). Similarly, the range size of the ancestral northern lineage of M. laminarioides (415 km) is smaller than that of the derived lineages; particularly, the southern lineage is much larger (“central” lineage range of 730 km; “south” lineage range of 2400 km; Table 10.1; Figs. 10.2 and 10.3; Montecinos et al. 2012). The unexpectedly large size of the recently diverged lineages in Mazzaella and Lessonia could be explained by recent post-speciation range shifts that do not reflect the historical range sizes of the lineages during the budding speciation process. Indeed, in the case of M. laminarioides, the “south” lineage has clearly been subjected to successive periods of range expansion/contraction during the glacial periods, which was not the case for the other two lineages that were located north of the glacial coverings (Montecinos et al. 2012). On the other hand, in plants for which clear evidence of range asymmetries support a scenario of budding speciation, the time of divergence between those sister species was determined to be very recent (less than 1 Myr, see for example Baldwin 2005 and Crawford et al. 2006). This does not seem to be the case for the studied seaweeds, and therefore current sister lineage distributions do not necessarily represent the range at budding speciation time for Mazzaella or Lessonia.
10.4.2 Genetic Diversity and Structure Within SEP Endemic Taxa
Regardless of the taxa studied, genetic differentiation was significant, confirming that seaweeds are generally poor dispersers compared to other marine organisms. Genetic estimates of dispersal distance in seaweeds are generally considered to be lower than 10 to 50 km (see reviews by Kinlan and Gaines 2003; Valero et al. 2011; Durrant et al. 2014). The minimum values of pairwise ΦST, observed for M. laminarioides “south”, were similar to values observed along the SEP coast for invertebrates with low dispersal capabilities (Haye et al. 2014). If dispersal is the main cause of the observed patterns of genetic differentiation, we would expect to find a significant relationship between genetic distances and geographic distances. Surprisingly, this was not the case for the three taxa of M. laminarioides studied, while isolation-by-distance (IBD) was significant for the three other taxa. For L. berteroana, L. spicata, M. laminarioides “north” and D. antarctica “central Chile” there is almost complete genetic isolation among populations separated by at most a few kilometres or tens of kilometres. It is probable that isolation-by-distance occurs at much shorter spatial scales than the species considered for the phylogeographic studies in these taxa.
The occurrence of haplotypes restricted to a few neighbouring populations and distributed in strict parapatry suggests that mechanisms other than limited dispersal may have contributed to such a patchy genetic diversity pattern. The mid to low intertidal habitat occupied by each of the studied species is intrinsically patchy since rocky shores along the SEP coast are interrupted by influential barriers, such as estuaries or sandy beaches (Thiel et al. 2007). Moreover, strong genetic drift is expected when populations are small and/or experience highly dynamic demographics and pass through periods of reduced population size. The combination of isolation and drift is strongly correlated with the level of genetic differentiation between pairs of populations in D. antarctica (Fraser et al. 2010a). In addition, strong demographic bottlenecks or local extinctions often occur in the region of the SEP located between 30°S and 40°S due to the recurrent effects of El Niño (Martínez et al. 2003; Thiel et al. 2007) and tectonic activity, which cause sudden changes to the elevation of the coast (Castilla 1988; Castilla et al. 2010; Jaramillo et al. 2012). If a local bottleneck is sufficiently strong, population recovery may be achieved by a reduced number of reproductively successful survivors or founders (in the case of local extinction). Such population dynamics typically reinforce the effects of genetic drift and may significantly contribute to patterns of genetic diversity and structure. The combined effects of reduced population size and high population turnover have been shown to reduce local genetic diversity and increase population genetic differentiation (Walser and Haag 2012). These effects can be observed even in species with high dispersive abilities such as floating seaweeds capable of rafting or species with long-lived spores. Considering gene flow restrictions when population densities reach a maximum, the Monopolization Hypothesis (De Meester et al. 2002; Waters et al. 2013) predicts that space will be saturated with local propagules soon after a bottleneck or a founder event, and this will give little chance for settlement of future immigrants. Under this hypothesis, dispersal is less efficient when patches of organisms are dense (Tellier et al. 2011a; Neiva et al. 2012 and for review see Waters et al. 2013). Moreover, the monopolization effect limits immigration therefore reinforcing local adaptation even if environmental heterogeneity in the system is minimal (De Meester et al. 2002). Under this scenario, historical phylogeographic disjunction patterns may last for long periods of time and can lead to speciation.
10.5 Post-glacial Histories: Distinguishing Between Local Population Recovery and Trans-oceanic Introductions
The phylogeographic literature on Patagonian species (i.e. south of 42°S) indicates complex and unexpected evolutionary histories. For terrestrial species, the high genetic diversityoften observed in Patagonia and the strong divergence among populations suggests ancient evolutionary processes that took place long before the LGM. Generally, it is proposed that populations persisted in different refugia in or around the glaciated region during the LGM (see Sérsic et al. 2011 for a review of 33 terrestrial plant and vertebrate species). Freshwater and marine animals seem to follow the same pattern. The use of periglacial refugia is hypothesized for frogs (Nuñez et al. 2011), fish (Ruzzante et al. 2008) and marine gastropods (Sánchez et al. 2011; González-Wevar et al. 2012) whereas glacially embedded refugia are hypothesized for fish (Zemlak et al. 2010), crabs (Xu et al. 2009) and river otters (Vianna et al. 2011).
In contrast, all the seaweed species studied to date show clear phylogeographic signatures of recent, post-glacial expansions in Patagonia. While haplotype networks are generally diversified and complex north of 42°S, only one or very few haplotypes have been detected in the region covered by the Patagonian ice sheet during the LGM (Fig. 10.2). A single haplotype is found in this region for the giant kelp Macrocystis pyrifera (Macaya and Zuccarello 2010a, b) and for the bull kelp D. antarctica (Fraser et al. 2009, 2010a, b), and a star-like haplotype network is observed in the red algae Gigartinaskottsbergii (Billard et al. 2015) and M. laminarioides “south” (Montecinos et al. 2012). It has generally not been possible to precisely estimate the timing of these demographic expansions due to a lack of accurate mutation rates for most molecular markers in seaweeds. However, the single haplotype shared by D. antarctica individuals found among all of the subantarctic islands and continental region of South America matches the latitudinal limits of coastal ice sheet coverage during the LGM (Fraser et al. 2009). This strongly suggests that the species colonized these areas only after the ice melted. In addition, the observation of a single haplotype strongly suggests that the subantarctic colonization is sufficiently recent that no new mutations have appeared in any of these regions. The large-scale spread of genetic variants has been observed during the recolonization of newly available empty habitats for both buoyant (D. antarctica, Fraser et al. 2010a; M. pyrifera, Alberto et al. 2010, 2011) and non-buoyant seaweeds (M. laminarioides, Faugeron et al. 2001; G. skottsbergii, Faugeron et al. 2004). During spatial expansion, gene surfing effects may contribute to the reduction of diversity in the recolonized region (Klopfstein et al. 2006; Hallatschek et al. 2007; Excoffier and Ray 2008; also see chapter by Neiva et al. (2016) in this volume). Indeed, gene surfing could lead to the presence of one or a few haplotypes over large recently colonized geographic areas (Klopfstein et al. 2006; Hallatschek et al. 2007; Excoffier and Ray 2008; Neiva et al. 2010). And finally, after the colonization of the region affected by ice, a density-blocking effect could have limited the establishment of new haplotypes allowing for the persistence of founder effect signatures long after spatial expansion is completed (De Meester et al. 2002; Waters et al. 2013). A better sampling coverage of the Magellan province and more polymorphic markers would be necessary to specifically test these various hypotheses.
Interestingly, there are two different hypothesized source populations for these post-glacial demographic expansions. One seems to be local, on the South American continent. In both M. laminarioides “south” and G. skottsbergii, population expansion apparently started from a single South American refuge. This conclusion is supported by the existence of a single central haplotype, shared by all populations, in the star-like networks of these two taxa (Fig. 10.2, Montecinos et al. 2012; Billard et al. 2015). Whereas it seems reasonable to think that the refugium was north of 42°S for M. laminarioides where most of the haplotype diversity is present, it is difficult to propose an exact location for the refuge of G.skottsbergii. For G. skottsbergii, the same central haplotype was found near the 42°S range limit, on the Southern tip of South America, and on the Falkland Islands, and no clear difference in haplotype diversity was observed over the whole species distribution range (41°–55°S). On the other hand, the source population of D. antarctica “subantarctic” for the post-glacial expansion in Chile was located in the New Zealand Subantarctic Islands (Fraser et al. 2009, 2010a, b). A similar scenario of recent transoceanic dispersal from New Zealand can also be inferred from the genetic diversity of the red alga Gracilaria chilensis (Guillemin et al. 2014). For ITS2, the only shared haplotype between both sides of the Pacific Ocean for G.chilensis was the central haplotype in the star-like network in Chile. This gives evidence for a recent population expansion after a founder effect due to the migration to Chile from New Zealand (Guillemin et al. 2014). One other seaweed shares its single Patagonian haplotype with subantarctic islands (South Georgia, Marion and Macquire), the giant kelp M. pyrifera (Macaya and Zuccarello 2010a, b). Because little diversity was found in mitochondrial sequences of M. pyrifera, it is difficult to infer the original source population of this subantarctic demographic expansion based on mtDNA phylogeography alone. Other genetic markers are required to make further inferences. Further discussion of trans-Pacific connectivity can be found in Chapter by Fraser (2016 in this volume). Moreover, more species should be studied to understand the history of the Magellan Province, which hosts high species richness despite the regular perturbations by glacial cycles.
10.6 Prospects and Challenges Ahead
Most seaweed phylogeographic studies show that the SEP coast houses a rich cryptic diversity. Of the 12 studies listed in Table 10.1, six have revealed the existence of crypticspecies or subspecies: in Lessonia (Tellier et al. 2009), Durvillaea (Fraser et al. 2009, 2010a, b), Adenocystis (Fraser et al. 2013), Mazzaella (Montecinos et al. 2012) and Nothogenia (Lindstrom et al. 2015). These results suggest that species diversity is underestimated in the region (see Peters et al. 2010; Fraser et al. 2013). Because the existence of high cryptic diversity could obscure biogeographic patterns (Riddle and Hafner 1999), future phylogeographic studies may lead to new biogeographic paradigms (for an example see the case of the Canadian Arctic marine flora in Saunders and McDevit 2013 where molecular data have allowed the authors to revisit hypotheses about the evolutionary origins and migration of algal taxa in this region). However, strong patterns have emerged from this first comparative study. First, different studies suggest parapatric and/or peripatric speciation occurs along the linear coast of SEP. Some speciation events seem to have taken place at the limit of the Intermediate Area and the Peruvian province (30–33°S). Yet other events of divergence do not correspond with any biogeographic limit or clear ecological barriers to gene flow. In this last case, the role of stochasticity associated with climatic and tectonic catastrophes needs to be further explored as a source of phylogeographic discontinuity. Moreover, in some morphospecies the location of phylogeographic discontinuities have not been clearly pinpointed due to logistical difficulties in accessing sites, which lead to large gaps in sampling. These gaps are most apparent in the Magellan province (between 44°S and 52°S, where access to the benthic habitat is impossible from land and very difficult by boat) and in the Peruvian province (i.e. between 18°S and 24°S, a region where few roads give access to the coast). Access to samples from these areas is essential to better assess species diversity along the SEP and test speciation or recolonization scenarios. Second, if population turnover is indeed high enough to promote genetic differentiation through founder and monopolization effects, effective dispersal is expected to be low. Dispersal and gene flow should be assessed at appropriate spatial scales to test this hypothesis. In the case of strong reductions in gene flow, even slight environmental differences may allow directional selection to promote local adaptation. This is an interesting perspective that future phylogeographic studies could include either through eco-physiological experimentation or by combining analyses of both neutral and selected markers using NGS technology and population genomics approaches (Beaumont and Balding 2004; Luikart et al. 2003). Third, several (cryptic) species actually colonized the SEP from New Zealand soon after the LGM. In this context, it could be interesting to investigate whether species diversity present along the SEP is the result of elevated local speciation rates (Center of Origin hypothesis) or rather due to the accumulation of species formed elsewhere (Center of Accumulation hypothesis; Briggs 2000; Barber 2009).
From a more applied point of view, these new phylogeographic results should lead to changes in management strategies and conservation of natural resources. Small fishing villages along the SEP sometimes heavily rely on algal communities as economically important resources. Both red (G. chilensis, Chondracanthus chamissoi, Pyropia spp., Sarcothalia crispata, M. laminarioidesand G. skottsbergii) and brown (Lessonia spp., D. antarctica and M. pyrifera) seaweeds are harvested along the coast (Buschmann et al. 2001; Guillemin et al. 2008; Vásquez 2008; Tellier et al. 2011b). Morpho-species with crypticdiversity should be taken into account when conservation and/or management programs are developed (Tellier et al. 2011b) if differences in population demographics or ecological niches lead to differing susceptibility to environmental threats. For example, ecological differences between L.berteroana and L. spicata in temperature and desiccation sensitivity (Oppliger et al. 2011, 2012; López-Cristoffanini et al. 2013) suggest that the species will experience different susceptibilities to events like ENSO. Finally, several species of algae are cultivated in Chile. Breeding strategies are emerging (Buschmann et al. 2014) and might face difficulties if reproductive barriers exist between cryptic species. Such reproductive isolation exists between L. spicata and L. berteroana in their overlapping distribution ranges (Tellier et al. 2011a). Taking into account the complex evolutionary processes occurring at large spatial and temporal scales is a necessity for these applied issues, and offers interesting perspectives of interactions among multiple research lines and disciplines.
This research was supported by CONICYT FONDECYT/REGULAR No. 1130797 and Centro FONDAP IDEAL No. 15150003 to MLG and FONDECYT/INICIACION No. 11121504 to FT. Additional support came from CONICYT PCCI/Proyectos de Intercambio No. PCCI130047, The Nucleo Milenio “Centro de Conservación Marina”—RC130004, the French Research Agency ANR-ECOKELP (ANR 06 BDIV 012) and International Research Network ‘‘Diversity, Evolution and Biotechnology of Marine Algae’’ (GDRI No. 0803).
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