Patterns of morphological diversification of mainland Anolis lizards from northwestern South America

Anolis lizards are one of the most diverse vertebrate genera and are the classic example of adaptive radiation and convergent evolution. Anoles exhibit great morphological diversity produced by the ecological opportunity to exploit several arboreal niches. Anole radiation in the Caribbean islands is well studied, but the mainland radiation is less understood. We used a large morphological data set and a molecular phylogeny to describe the morphological diversification of anoles from northwestern South America, a region with the highest anole diversity on a mainland. We describe morphological diversity as summarized by ten morphotypes, defined mainly by body size, limb proportions, and subdigital lamellae. We show that some morphotypes are limited to forested lowlands and others to Andean highlands; by contrast, Anolis assemblages from tropical rainforests are comprised of the same four morphotypes. We demonstrate that morphological diversification followed a pattern of adaptive radiation across a landscape of adaptive peaks. Our results are consistent with the most recent hypothesis of convergence stated for Caribbean radiation, and demonstrate convergence between mainland morphotypes and Caribbean ecomorphs, which suggests that common processes are driving both radiations. © 2016 The Linnean Society of London     

Novel trophic niches drive variable progress towards ecological speciation within an adaptive radiation of pupfishes

Adaptive radiation is recognized by a rapid burst of phenotypic, ecological and species diversification. However, it is unknown whether different species within an adaptive radiation evolve reproductive isolation at different rates. We compared patterns of genetic differentiation between nascent species within an adaptive radiation of Cyprinodon pupfishes using genotyping by sequencing. Similar to classic adaptive radiations, this clade exhibits rapid morphological diversification rates and two species are novel trophic specialists, a scale‐eater and hard‐shelled prey specialist (durophage), yet the radiation is <10 000 years old. Both specialists and an abundant generalist species all coexist in the benthic zone of lakes on San Salvador Island, Bahamas. Based on 13 912 single‐nucleotide polymorphisms (SNPs), we found consistent differences in genetic differentiation between each specialist species and the generalist across seven lakes. The scale‐eater showed the greatest genetic differentiation and clustered by species across lakes, whereas durophage populations often clustered with sympatric generalist populations, consistent with parallel speciation across lakes. However, we found strong evidence of admixture between durophage populations in different lakes, supporting a single origin of this species and genome‐wide introgression with sympatric generalist populations. We conclude that the scale‐eater is further along the speciation‐with‐gene‐flow continuum than the durophage and suggest that different adaptive landscapes underlying these two niche environments drive variable progress towards speciation within the same habitat. Our previous measurements of fitness surfaces in these lakes support this conclusion: the scale‐eating fitness peak may be more distant than the durophage peak on the complex adaptive landscape driving adaptive radiation.     

Phylogeographic and phenotypic outcomes of brown anole colonization across the Caribbean provide insight into the beginning stages of an adaptive radiation

Some of the most important insights into the ecological and evolutionary processes of diversification and speciation have come from studies of island adaptive radiations, yet relatively little research has examined how these radiations initiate. We suggest that Anolis sagrei is a candidate for understanding the origins of the Caribbean Anolis adaptive radiation and how a colonizing anole species begins to undergo allopatric diversification, phenotypic divergence and, potentially, speciation. We undertook a genomic and morphological analysis of representative populations across the entire native range of A. sagrei, finding that the species originated in the early Pliocene, with the deepest divergence occurring between western and eastern Cuba. Lineages from these two regions subsequently colonized the northern Caribbean. We find that at the broadest scale, populations colonizing areas with fewer closely related competitors tend to evolve larger body size and more lamellae on their toepads. This trend follows expectations for post‐colonization divergence from progenitors and convergence in allopatry, whereby populations freed from competition with close relatives evolve towards common morphological and ecological optima. Taken together, our results show a complex history of ancient and recent Cuban diaspora with populations on competitor‐poor islands evolving away from their ancestral Cuban populations regardless of their phylogenetic relationships, thus providing insight into the original diversification of colonist anoles at the beginning of the radiation. Our research also supplies an evolutionary framework for the many studies of this increasingly important species in ecological and evolutionary research.     

Ecological opportunity and the origin of adaptive radiations

Ecological opportunity – through entry into a new environment, the origin of a key innovation or extinction of antagonists – is widely thought to link ecological population dynamics to evolutionary diversification. The population‐level processes arising from ecological opportunity are well documented under the concept of ecological release. However, there is little consensus as to how these processes promote phenotypic diversification, rapid speciation and adaptive radiation. We propose that ecological opportunity could promote adaptive radiation by generating specific changes to the selective regimes acting on natural populations, both by relaxing effective stabilizing selection and by creating conditions that ultimately generate diversifying selection. We assess theoretical and empirical evidence for these effects of ecological opportunity and review emerging phylogenetic approaches that attempt to detect the signature of ecological opportunity across geological time. Finally, we evaluate the evidence for the evolutionary effects of ecological opportunity in the diversification of Caribbean Anolis lizards. Some of the processes that could link ecological opportunity to adaptive radiation are well documented, but others remain unsupported. We suggest that more study is required to characterize the form of natural selection acting on natural populations and to better describe the relationship between ecological opportunity and speciation rates.     

HOST‐SPECIALIST LINEAGES DOMINATE THE ADAPTIVE RADIATION OF REEF CORAL ENDOSYMBIONTS

Bursts in species diversification are well documented among animals and plants, yet few studies have assessed recent adaptive radiations of eukaryotic microbes. Consequently, we examined the radiation of the most ecologically dominant group of endosymbiotic dinoflagellates found in reef‐building corals, Symbiodinium Clade C, using nuclear ribosomal (ITS2), chloroplast (psbA^ncr), and multilocus microsatellite genotyping. Through a hierarchical analysis of high‐resolution genetic data, we assessed whether ecologically distinct Symbiodinium, differentiated by seemingly equivocal rDNA sequence differences, are independent species lineages. We also considered the role of host specificity in Symbiodinium speciation and the correspondence between endosymbiont diversification and Caribbean paleo‐history. According to phylogenetic, biological, and ecological species concepts, Symbiodinium Clade C comprises many distinct species. Although regional factors contributed to population‐genetic structuring of these lineages, Symbiodinium diversification was mainly driven by host specialization. By combining patterns of the endosymbiont's host specificity, water depth distribution, and phylogeography with paleo‐historical signals of climate change, we inferred that present‐day species diversity on Atlantic coral reefs stemmed mostly from a post‐Miocene adaptive radiation. Host‐generalist progenitors spread, specialized, and diversified during the ensuing epochs of prolonged global cooling and change in reef‐faunal assemblages. Our evolutionary reconstruction thus suggests that Symbiodinium undergoes “boom and bust” phases in diversification and extinction during major climate shifts.     

Relaxed trait covariance in interspecific cichlid hybrids predicts morphological diversity in adaptive radiations

The process of adaptive radiation involves multiple events of speciation in short succession, associated with ecological diversification. Understanding this process requires identifying the origins of heritable phenotypic variation that allows adaptive radiation to progress. Hybridization is one source of genetic and morphological variation that may spur adaptive radiation. We experimentally explored the potential role of hybridization in facilitating the onset of adaptive radiation. We generated first‐ and second‐generation hybrids of four species of African cichlid fish, extant relatives of the putative ancestors of the adaptive radiations of Lakes Victoria and Malawi. We compared patterns in hybrid morphological variation with the variation in the lake radiations. We show that significant fractions of the interspecific morphological variation and the major trajectories in morphospace that characterize whole radiations can be generated in second‐generation hybrids. Furthermore, we show that covariation between traits is relaxed in second‐generation hybrids, which may facilitate adaptive diversification. These results support the idea that hybridization can provide the heritable phenotypic diversity necessary to initiate adaptive radiation.     

Equilibrium and non‐equilibrium dynamics simultaneously operate in the Galápagos islands

Island biotas emerge from the interplay between colonisation, speciation and extinction and are often the scene of spectacular adaptive radiations. A common assumption is that insular diversity is at a dynamic equilibrium, but for remote islands, such as Hawaii or Galápagos, this idea remains untested. Here, we reconstruct the temporal accumulation of terrestrial bird species of the Galápagos using a novel phylogenetic method that estimates rates of biota assembly for an entire community. We show that species richness on the archipelago is in an ascending phase and does not tend towards equilibrium. The majority of the avifauna diversifies at a slow rate, without detectable ecological limits. However, Darwin's finches form an exception: they rapidly reach a carrying capacity and subsequently follow a coalescent‐like diversification process. Together, these results suggest that avian diversity of remote islands is rising, and challenge the mutual exclusivity of the non‐equilibrium and equilibrium ecological paradigms.     

Hybridization and adaptive radiation

Whether interspecific hybridization is important as a mechanism that generates biological diversity is a matter of controversy. Whereas some authors focus on the potential of hybridization as a source of genetic variation, functional novelty and new species, others argue against any important role, because reduced fitness would typically render hybrids an evolutionary dead end. By drawing on recent developments in the genetics and ecology of hybridization and on principles of ecological speciation theory, I develop a concept that reconciles these views and adds a new twist to this debate. Because hybridization is common when populations invade new environments and potentially elevates rates of response to selection, it predisposes colonizing populations to rapid adaptive diversification under disruptive or divergent selection. I discuss predictions and suggest tests of this hybrid swarm theory of adaptive radiation and review published molecular phylogenies of adaptive radiations in light of the theory.     

Trophic novelty is linked to exceptional rates of morphological diversification in two adaptive radiations of Cyprinodon pupfish

Adaptive radiations are known for rapid morphological and species diversification in response to ecological opportunity, but it remains unclear if distinct mechanisms drive this pattern. Here, we show that rapid rates of morphological diversification are linked to the evolution of novel ecological niches in two independent Cyprinodon radiations nested within a wide-ranging group repeatedly isolated in extreme environments. We constructed a molecular phylogeny for the Cyprinodontidae, measured 16 functional traits across this group, and compared the likelihoods of single or multiple rates of morphological diversification. We found that rates of morphological diversification within two sympatric Cyprinodon clades containing unique trophic specialists are not part of an adaptive continuum with other clades, but are instead extreme outliers with rates up to 131 times faster than other Cyprinodontidae. High rates were not explained by clade age, but were instead linked to unique trophic niches within Cyprinodon, including scale-eating, zooplanktivory, and piscivory. Furthermore, although both radiations occur in similar environments and have similar sister species, they each evolved unique trophic specialists and high rates of morphological diversification in different sets of traits. We propose that the invasion of novel ecological niches may be a key mechanism driving many classic examples of adaptive radiation.     

Ecomorphological diversification following continental colonization in muroid rodents (Rodentia: Muroidea)

The emergence of exceptionally diverse clades is often attributed to ecological opportunity. For example, the exceptional diversity in the most diverse superfamily of mammals, muroid rodents, has been explained in terms of multiple independent adaptive radiations. If multiple ecological opportunity events are responsible for generating muroid diversity, we expect to find evidence of these lineages ecologically diversifying following dispersal into new biogeographical areas. In the present study, we tested the trait‐based predictions of ecological opportunity using data on body size, appendages, and elevation in combination with previously published data on biogeographical transitions and a time‐calibrated molecular phylogeny. We identified weak to no support of early ecological diversification following the initial colonizations of all continental regions, based on multiple tests, including node height tests, disparity through time plots, evolutionary model comparison, and Bayesian analysis of macroevolutionary mixtures. Clades identified with increased diversification rates, not associated with geographical transitions, also did not show patterns of phenotypic divergence predicted by ecological opportunity, which suggests that phylogenetic diversity and phenotypic disparity may be decoupled in muroids. These results indicate that shifts in diversification rates and biogeographically‐mediated ecological opportunity are poor predictors of phenotypic diversity patterns in muroids.     

AN ADAPTIVE RADIATION OF FROGS IN A SOUTHEAST ASIAN ISLAND ARCHIPELAGO

Living amphibians exhibit a diversity of ecologies, life histories, and species‐rich lineages that offers opportunities for studies of adaptive radiation. We characterize a diverse clade of frogs (Kaloula, Microhylidae) in the Philippine island archipelago as an example of an adaptive radiation into three primary habitat specialists or ecotypes. We use a novel phylogenetic estimate for this clade to evaluate the tempo of lineage accumulation and morphological diversification. Because species‐level phylogenetic estimates for Philippine Kaloula are lacking, we employ dense population sampling to determine the appropriate evolutionary lineages for diversification analyses. We explicitly take phylogenetic uncertainty into account when calculating diversification and disparification statistics and fitting models of diversification. Following dispersal to the Philippines from Southeast Asia, Kaloula radiated rapidly into several well‐supported clades. Morphological variation within Kaloula is partly explained by ecotype and accumulated at high levels during this radiation, including within ecotypes. We pinpoint an axis of morphospace related directly to climbing and digging behaviors and find patterns of phenotypic evolution suggestive of ecological opportunity with partitioning into distinct habitat specialists. We conclude by discussing the components of phenotypic diversity that are likely important in amphibian adaptive radiations.     

Apparent signal of competition limiting diversification after ecological transitions from marine to freshwater habitats

Adaptive radiations are typically triggered when a lineage encounters a significant range of open niche space (ecological opportunity), stemming from colonisation of new areas, extinction of competitors or key innovations. The most well-known of these is the colonisation of new areas, through either dispersal into new regions or the invasion of novel ecological regimes. One aspect of ecological opportunity that has rarely been studied, however, is the extent to which pre-existent competitors act to limit diversification in newly colonised adaptive zones. Herein, we show that in multiple geographically independent invasions of freshwaters by marine Sea Catfishes (Ariidae), rates of both morphological disparification and lineage diversification are inversely related to the presence and diversity of other freshwater fish lineages. Only in one region (Australia-New Guinea) with an otherwise depauperate freshwater fauna, has an ariid invasion gained any substantial traction. This is true at both regional and community scales, suggesting that competitive constraints may be an important factor regulating adaptive radiation.     

Adaptive radiation in labrid fishes: A central role for functional innovations during 65 My of relentless diversification

Early burst patterns of diversification have become closely linked with concepts of adaptive radiation, reflecting interest in the role of ecological opportunity in modulating diversification. But, this model has not been widely explored on coral reefs, where biodiversity is exceptional, but many lineages have high dispersal capabilities and a pan‐tropical distribution. We analyze adaptive radiation in labrid fishes, arguably the most ecologically dominant and diverse radiation of fishes on coral reefs. We test for time‐dependent speciation, trophic diversification, and origination of 15 functional innovations, and early bursts in a series of functional morphological traits associated with feeding and locomotion. We find no evidence of time‐dependent or early burst evolution. Instead, the pace of speciation, ecological diversification, and trait evolution has been relatively constant. The origination of functional innovations has slowed over time, although few arose early. The labrid radiation seems to have occurred in response to extensive and still increasing ecological opportunity, but within a rich community of antagonists that may have prevented abrupt diversification. Labrid diversification is closely tied to a series of substantial functional innovations that individually broadened ecological diversity, ultimately allowing them to invade virtually every trophic niche held by fishes on coral reefs.     

When are adaptive radiations replicated in areas? Ecological opportunity and unexceptional diversification in West Indian dipsadine snakes (Colubridae: Alsophiini)

Aim We examine diversification in Caribbean alsophiine snakes and hypothesize that, given the ecological opportunity presented by colonization of the West Indies, alsophiines should show the signature of an early burst of diversification and associated low within‐clade ecological and morphological disparification. We also test whether changes in morphology and ecology are associated with changes in diversification rate, as trait‐dependent diversification is hypothesized to affect historical inferences of diversification and disparification. Finally, as replicated radiations are found across the West Indies in the anoles, we test for significant differences in ecological and morphological assemblages and rates among the major island groups. Location The West Indies. Methods A time‐calibrated phylogeny produced from six genes using relaxed clock methods in beast was constructed to estimate ancestral areas using Lagrange . Maximum body size and ecological niche were scored for all species in the phylogeny, and comparative phylogenetic methods in R using geiger , laser , ape and our own code were used to examine diversification through time, disparification and trait‐dependent diversification from this dated phylogeny. Results The pattern of species diversification did not differ significantly from the Yule model of diversification. Morphology and ecology fitted a Brownian and white noise model of diversification, respectively. Although not significantly different, morphological disparification was lower than the Brownian null model, whereas ecological disparification was significantly greater than the null. Trait‐dependent diversification analyses suggested that the constant null models provided the best fit to these data. There was no significant signal of rate variation among the major island groups for size, but moderate evidence for niche. Main conclusions Although ecological opportunity was similarly present for alsophiines as it was for anoles, the snakes fail to show an early burst of speciation. Potential reasons for this include the young age of the group, and staggered diversification due to waiting times between island colonization. In turn, ecological and morphological disparities do not necessarily follow predictable patterns related to species diversification. Thus, the presence of ecological opportunity alone is not necessarily sufficient to trigger replicated adaptive radiations in areas.     

Renewed diversification is associated with new ecological opportunity in the Neotropical turtle ants

Ecological opportunity, defined as access to new resources free from competitors, is thought to be a catalyst for the process of adaptive radiation. Much of what we know about ecological opportunity, and the larger process of adaptive radiation, is derived from vertebrate diversification on islands. Here, we examine lineage diversification in the turtle ants (Cephalotes), a species‐rich group of ants that has diversified throughout the Neotropics. We show that crown group turtle ants originated during the Eocene (around 46 mya), coincident with global warming and the origin of many other clades. We also show a marked lineage‐wide slowdown in diversification rates in the Miocene. Contrasting this overall pattern, a species group associated with the young and seasonally harsh Chacoan biogeographic region underwent a recent burst of diversification. Subsequent analyses also indicated that there is significant phylogenetic clustering within the Chacoan region and that speciation rates are highest there. Together, these findings suggest that recent ecological opportunity, from successful colonization of novel habitat, may have facilitated renewed turtle ant diversification. Our findings highlight a central role of ecological opportunity within a successful continental radiation.     

A preliminary classification of evolutionary radiations

Rapid increases in taxonomic diversity are generally described as adaptive or evolutionary radiations. Such radiations differ widely in the rate and extent of morphologic innovation, taxonomic diversification and phylogenetic breadth, suggesting that several patterns, and likely processes, are involved. At least four distinct patterns of evolutionary radiation can be identified: novelty events, which generate new morphological complexity (altering the body plan of the group under consideration) but not necessarily with the associated production of many lower taxa; broad diversification events involving many independent lineages that undergo diversification, generate many new species and are driven by new ecological opportunities; economic radiations of a limited group of ecologically (but not necessarily phylogenetically) related clades exploiting a limited new ecologic opportunity; and adaptive radiations that may occur at any taxonomic level, but involve a rapid increase in diversity within a single clade, including “true”; adaptive radiations. Many events produce simple diversity increases with no corresponding increase in genetic/developmental/morphological/behavioral sophistication, but the most evolutionarily interesting events add new levels of complexity.     

Radiating on oceanic islands: patterns and processes of speciation in the land snail genus Theba (Risso 1826)

Island radiations have played a major role in shaping our current understanding of allopatric, sympatric and parapatric speciation. However, the fact that species divergence correlates with island size emphasizes the importance of geographic isolation (allopatry) in speciation. Based on molecular and morphological data, we investigated the diversification of the land snail genus Theba on the two Canary Islands of Lanzarote and Fuerteventura. Due to the geological history of both islands, this study system provides ideal conditions to investigate the interplay of biogeography, dispersal ability and differentiation in generating species diversity. Our analyses demonstrated extensive cryptic diversification of Theba on these islands, probably driven mainly by non-adaptive allopatric differentiation and secondary gene flow. In a few cases, we observed a complete absence of gene flow among sympatrically distributed forms suggesting an advanced stage of speciation. On the Jandía peninsula genome scans suggested genotype-environment associations and potentially adaptive diversification of two closely related Theba species to different ecological environments. We found support for the idea that genetic differentiation was enhanced by divergent selection in different environments. The diversification of Theba on both islands is therefore best explained by a mixture of non-adaptive and adaptive speciation, promoted by ecological and geomorphological factors.     

Ecomorphological convergence in Eleutherodactylus frogs: a case of replicate radiations in the Caribbean

Replicate radiations, the repeated multiplication of species associated with ecological divergence, have attracted much attention and generated as much debate. Due to the few well‐studied cases, it remains unclear whether replicate radiations are an exceptional result of evolution or a relatively common example of the power of adaptation by natural selection. We examined the case of Eleutherodactylus frogs, which radiated in the Caribbean islands resulting in more than 160 species that occupy very diverse habitats. A time‐calibrated phylogeny revealed that these frogs independently diversified on all larger islands producing species that occupy a broad range of microhabitats in different islands. Using phylogenetic comparative methods, we found an association between morphological traits and particular microhabitats, and for most microhabitats detected significant morphological convergence. Our results indicate Caribbean Eleutherodactylus are a novel example of replicate radiations, and highlight the predictability of evolutionary processes, as similar ecological opportunities can lead to similar outcomes.     

THE EVOLUTIONARY HISTORY OF DARWIN'S FINCHES: SPECIATION,GENE FLOW,AND INTROGRESSION IN A FRAGMENTED LANDSCAPE

Many classic examples of adaptive radiations take place within fragmented systems such as islands or mountains, but the roles of mosaic landscapes and variable gene flow in facilitating species diversification is poorly understood. Here we combine phylogenetic and landscape genetic approaches to understand diversification in Darwin's finches, a model adaptive radiation. We combined sequence data from 14 nuclear introns, mitochondrial markers, and microsatellite variation from 51 populations of all 15 recognized species. Phylogenetic species‐trees recovered seven major finch clades: ground, tree, vegetarian, Cocos Island, grey and green warbler finches, and a distinct clade of sharp‐beaked ground finches (Geospiza cf. difficilis) basal to all ground and tree finches. The ground and tree finch clades lack species‐level phylogenetic structure. Interisland gene flow and interspecies introgression vary geographically in predictable ways. First, several species exhibit concordant patterns of population divergence across the channel separating the Galápagos platform islands from the separate volcanic province of northern islands. Second, peripheral islands have more admixed populations while central islands maintain more distinct species boundaries. This landscape perspective highlights a likely role for isolation of peripheral populations in initial divergence, and demonstrates that peripheral populations may maintain genetic diversity through outbreeding during the initial stages of speciation.     

TESTING FOR ANCIENT ADAPTIVE RADIATIONS IN NEOTROPICAL CICHLID FISHES

Most contemporary studies of adaptive radiation focus on relatively recent and geographically restricted clades. It is less clear whether diversification of ancient clades spanning entire continents is consistent with adaptive radiation. We used novel fossil calibrations to generate a chronogram of Neotropical cichlid fishes and to test whether patterns of lineage and morphological diversification are congruent with hypothesized adaptive radiations in South and Central America. We found that diversification in the Neotropical cichlid clade and the highly diverse tribe Geophagini was consistent with diversity‐dependent, early bursts of divergence followed by decreased rates of lineage accumulation. South American Geophagini underwent early rapid differentiation in body shape, expanding into novel morphological space characterized by elongate‐bodied predators. Divergence in head shape attributes associated with trophic specialization evolved under strong adaptive constraints in all Neotropical cichlid clades. The South American Cichlasomatini followed patterns consistent with constant rates of morphological divergence. Although morphological diversification in South American Heroini was limited, Eocene invasion of Central American habitats was followed by convergent diversification mirroring variation observed in Geophagini. Diversification in Neotropical cichlids was influenced by the early adaptive radiation of Geophagini, which potentially limited differentiation in other cichlid clades.