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.     

Recent and rapid speciation with limited morphological disparity in the genus Rattus

Recent and rapid radiations provide rich material to examine the factors that drive speciation. Most recent and rapid radiations that have been well-characterized involve species that exhibit overt ecomorphological differences associated with clear partitioning of ecological niches in sympatry. The most diverse genus of rodents, Rattus (66 species), evolved fairly recently, but without overt ecomorphological divergence among species. We used multilocus molecular phylogenetic data and five fossil calibrations to estimate the tempo of diversification in Rattus, and their radiation on Australia and New Guinea (Sahul, 24 species). Based on our analyses, the genus Rattus originated at a date centered on the Pliocene-Pleistocene boundary (1.84-3.17 Ma) with a subsequent colonization of Sahul in the middle Pleistocene (0.85-1.28 Ma). Given these dates, the per lineage diversification rates in Rattus and Sahulian Rattus are among the highest reported for vertebrates (1.1-1.9 and 1.6-3.0 species per lineage per million years, respectively). Despite their rapid diversification, Rattus display little ecomorphological divergence among species and do not fit clearly into current models of adaptive radiations. Lineage through time plots and ancestral state reconstruction of ecological characters suggest that diversification of Sahulian Rattus was most rapid early on as they expanded into novel ecological conditions. However, rapid lineage accumulation occurred even when morphological disparity within lineages was low suggesting that future studies consider other phenotypes in the diversification of Rattus.     

Understanding the effect of competition during evolutionary radiations: an integrated model of phenotypic and species diversification

Competition can drive macroevolutionary change, for example during adaptive radiations. However, we still lack a clear understanding of how it shapes diversification processes and patterns. To better understand the macroevolutionary consequences of competition, as well as the signal left on phylogenetic data, we developed a model linking trait evolution and species diversification in an ecological context. We find four main results: first, competition spurs trait diversity but not necessarily species richness; second, competition produces slowdowns in species diversification even in the absence of explicit ecological limits, but not in phenotypic diversification even in the presence of such limits; third, early burst patterns do not provide a reliable way of testing for adaptive radiations; and fourth, looking for phylogenetic signal in trait data and support for phenotypic models incorporating competition is a better alternative. Our results clarify the macroevolutionary consequences of competition and could help design more powerful tests of adaptive radiations in nature.     

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.     

Phylogeny of Saxifragales (angiosperms,eudicots): analysis of a rapid,ancient radiation

Rapid, ancient radiations pose one of the most difficult challenges for phylogenetic estimation. We used DNA sequence data of 9,006 aligned base pairs from five genes (chloroplast atpB, matK, rbcL, and 18S and 26S nrDNA) to elucidate relationships among major lineages of Saxifragales (angiosperms, eudicots). These relationships were poorly supported in previous studies, apparently because the lineages originated in rapid succession. Using an array of methods that explicitly incorporate assumptions about evolutionary process (weighted maximum parsimony, maximum likelihood, LogDet/paralinear transformed distances), we show that the initial diversification of Saxifragales was indeed rapid. We suggest that the poor resolution of our best phylogenetic estimate is not due to violations of assumptions or to combining data partitions having conflicting histories or processes. We show that estimated branch lengths during the initial diversification are exceedingly short, and we estimate that acquiring sufficient sequence data to resolve these relationships would require an extraordinary effort (approximately 10(7) bp), assuming a linear increase in branch support with branch length. However, our simulation of much larger data sets containing a distribution of phylogenetic signal similar to that of the five sampled gene sequences suggests a limit to achievable branch support. Using statistical tests of differences in the likelihoods of topologies, we evaluated whether the initial radiation of Saxifragales involved the simultaneous origin of major lineages. Our results are consistent with predictions that resolving the branching order of rapid, ancient radiations requires sampling characters that evolved rapidly at the time of the radiation but have since experienced a slower evolutionary rate.     

Phylogeny estimation of the radiation of western North American chipmunks (Tamias) in the face of introgression using reproductive protein genes

The causes and consequences of rapid radiations are major unresolved issues in evolutionary biology. This is in part because phylogeny estimation is confounded by processes such as stochastic lineage sorting and hybridization. Because these processes are expected to be heterogeneous across the genome, comparison among marker classes may provide a means of disentangling these elements. Here we use introns from nuclear-encoded reproductive protein genes expected to be resistant to introgression to estimate the phylogeny of the western chipmunks (Tamias: subgenus: Neotamias), a rapid radiation that has experienced introgressive hybridization of mitochondrial DNA (mtDNA). We analyze the nuclear loci using coalescent-based species-tree estimation methods and concatenation to estimate a species tree and we use parametric bootstraps and coalescent simulations to differentiate between phylogenetic error, coalescent stochasticity and introgressive hybridization. Results indicate that the mtDNA gene tree reflects several introgression events that have occurred between taxa of varying levels of divergence and at different time points in the tree. T. panamintinus and T. speciosus appear to be fixed for ancient mitochondrial introgressions from T. minimus. A southern Rocky Mountains clade appears well sorted (i.e., species are largely monophyletic) at multiple nuclear loci, while five of six taxa are nonmonophyletic based on cytochrome b. Our simulations reject phylogenetic error and coalescent stochasticity as causes. The results represent an advance in our understanding of the processes at work during the radiation of Tamias and suggest that sampling reproductive-protein genes may be a viable strategy for phylogeny estimation of rapid radiations in which reproductive isolation is incomplete. However, a genome-scale survey that can statistically compare heterogeneity of genealogical process at many more loci will be necessary to test this conclusion.     

PHYLOGENETIC,ECOLOGICAL, AND ALLOMETRIC CORRELATES OF CRANIAL SHAPE IN MALAGASY LEMURIFORMS

Adaptive radiations provide important insights into many aspects of evolution, including the relationship between ecology and morphological diversification as well as between ecology and speciation. Many such radiations include divergence along a dietary axis, although other ecological variables may also drive diversification, including differences in diel activity patterns. This study examines the role of two key ecological variables, diet and activity patterns, in shaping the radiation of a diverse clade of primates, the Malagasy lemurs. When phylogeny was ignored, activity pattern and several dietary variables predicted a significant proportion of cranial shape variation. However, when phylogeny was taken into account, only typical diet accounted for a significant proportion of shape variation. One possible explanation for this discrepancy is that this radiation was characterized by a relatively small number of dietary shifts (and possibly changes in body size) that occurred in conjunction with the divergence of major clades. This pattern may be difficult to detect with the phylogenetic comparative methods used here, but may characterize not just lemurs but other mammals.     

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.     

A climate for speciation: rapid spatial diversification within the Sorex cinereus complex of shrews

The cyclic climate regime of the late Quaternary caused dramatic environmental change at high latitudes. Although these events may have been brief in periodicity from an evolutionary standpoint, multiple episodes of allopatry and divergence have been implicated in rapid radiations of a number of organisms. Shrews of the Sorex cinereus complex have long challenged taxonomists due to similar morphology and parapatric geographic ranges. Here, multi-locus phylogenetic and demographic assessments using a coalescent framework were combined to investigate spatiotemporal evolution of 13 nominal species with a widespread distribution throughout North America and across Beringia into Siberia. For these species, we first test a hypothesis of recent differentiation in response to Pleistocene climate versus more ancient divergence that would coincide with pre-Pleistocene perturbations. We then investigate the processes driving diversification over multiple continents. Our genetic analyses highlight novel diversity within these morphologically conserved mammals and clarify relationships between geographic distribution and evolutionary history. Demography within and among species indicates both regional stability and rapid expansion. Ancestral ecological differentiation coincident with early cladogenesis within the complex enabled alternating and repeated episodes of allopatry and expansion where successive glacial and interglacial phases each promoted divergence. The Sorex cinereus complex constitutes a valuable model for future comparative assessments of evolution in response to cyclic environmental change.     

Heads or tails: staged diversification in vertebrate evolutionary radiations

Adaptive radiations, bouts of morphological divergence coupled with taxonomic proliferation, underpin biodiversity. The most widespread model of radiations assumes a single round, or 'early burst', of elevated phenotypic divergence followed by a decline in rates of change or even stasis. A vertebrate-specific model proposes separate stages: initial divergence in postcranial traits related to habitat use, followed by diversification in cranial morphology linked to trophic demands. However, there is little empirical evidence for either hypothesis. Here, we show that, contrary to both models, separate large-scale radiations of actinopterygian fishes proceeded through distinct cranial and later postcranial stages of morphological diversification. Early actinopterygians and acanthomorph teleosts dispersed in cranial morphospace immediately following the end-Devonian extinction and the Cretaceous origin of the acanthomorph clade, respectively. Significant increases in postcranial morphological variation do not occur until one interval after cranial diversification commenced. Therefore, our results question the universality of the 'general vertebrate model'. Based on the results of model-fitting exercises and application of the divergence order test, we find little evidence that the early onset of cranial diversification in these two radiations is due to elevated rates of cranial change relative to postcranial change early in their evolutionary histories. Instead, postcranial and cranial patterns are best fit by an Ornstein-Uhlenbeck model, which is characterized by constant evolutionary rates coupled with a strong central tendency. Other groups have been reported to show early saturation of cranial morphospace or tropic roles early in their histories, but it is unclear whether these patterns are attributable to dynamics similar to those inferred for our two model radiations.     

Rapid lineage accumulation in a non-adaptive radiation: phylogenetic analysis of diversification rates in eastern North American woodland salamanders (Plethodontidae: Plethodon)

Adaptive radiations have served as model systems for quantifying the build-up of species richness. Few studies have quantified the tempo of diversification in species-rich clades that contain negligible adaptive disparity, making the macroevolutionary consequences of different modes of evolutionary radiation difficult to assess. We use mitochondrial-DNA sequence data and recently developed phylogenetic methodologies to explore the tempo of diversification of eastern North American Plethodon, a species-rich clade of woodland salamanders exhibiting only limited phenotypic disparity. Lineage-through-time analysis reveals a high rate of lineage accumulation, 0.8 species per million years, occurring 11-8 million years ago in the P. glutinosus species group, followed by decreasing rates. This high rate of lineage accumulation is exceptional, comparable to the most rapid of adaptive radiations. In contrast to classic models of adaptive radiation where ecological niche divergence is linked to the origin of species, we propose that phylogenetic niche conservatism contributes to the rapid accumulation of P. glutinosus-group lineages by promoting vicariant isolation and multiplication of species across a spatially and temporally fluctuating environment. These closely related and ecologically similar lineages persist through long-periods of evolutionary time and form strong barriers to the geographic spread of their neighbours, producing a subsequent decline in lineage accumulation. Rapid diversification among lineages exhibiting long-term maintenance of their bioclimatic niche requirements is an under-appreciated phenomenon driving the build-up of species richness.     

Evolutionary radiation of "stone plants" in the genus Argyroderma (Aizoaceae): unraveling the effects of landscape, habitat, and flowering time

Recent phylogenetic evidence suggests that the extraordinary diversity of the Cape Floristic Kingdom in South Africa may be the result of widespread evolutionary radiation. Our understanding of the role of adaptive versus neutral processes in these radiations remains largely speculative. In this study we investigated factors involved in the diversification of Argyroderma, a genus within the most spectacular of the Cape radiations, that of the Ruschioid subfamily of the Aizoaceae. We used amplified fragment length polymorphisms and a suite of morphological traits to elucidate patterns of differentiation within and between species of Argyroderma across the range of the genus. We then used a matrix correlation approach to assess the influence of landscape structure, edaphic gradients, and flowering phenology on phenotypic and neutral genetic divergence in the system. We found evidence for strong spatial genetic isolation at all taxonomic levels. In addition, genetic differentiation occurs along a temporal axis, between sympatric species with divergent flowering times. Morphological differentiation, which previous studies suggest is adaptive, occurs along a habitat axis, between populations occupying different edaphic microenvironments. Morphological differentiation is in turn significantly associated with flowering time shifts. Thus we propose that diversification within Argyroderma has occurred through a process of adaptive speciation in allopatry. Spatially isolated populations diverge phenotypically in response to divergent habitat selection, which in turn leads to the evolution of reproductive isolation through divergence of flowering phenologies, perhaps as a correlated response to morphological divergence. Evidence suggests that diversification of the group has proceeded in two phases: the first involving divergence of allopatric taxa on varied microhabitats within a novel habitat type (the quartz gravel plains), and the second involving range expansion of an early flowering phenotype on the most extreme edaphic habitat and subsequent incomplete differentiation of allopatric populations of the early flowering group. These results point to adaptive speciation in allopatry as a likely model for the spectacular diversification of the ice-plant family in the dissected landscapes of the southern African winter rainfall deserts.     

Polyploidy and angiosperm diversification

Polyploidy has long been recognized as a major force in angiosperm evolution. Recent genomic investigations not only indicate that polyploidy is ubiquitous among angiosperms, but also suggest several ancient genome-doubling events. These include ancient whole genome duplication (WGD) events in basal angiosperm lineages, as well as a proposed paleohexaploid event that may have occurred close to the eudicot divergence. However, there is currently no evidence for WGD in Amborella, the putative sister species to other extant angiosperms. The question is no longer "What proportion of angiosperms are polyploid?", but "How many episodes of polyploidy characterize any given lineage?" New algorithms provide promise that ancestral genomes can be reconstructed for deep divergences (e.g., it may be possible to reconstruct the ancestral eudicot or even the ancestral angiosperm genome). Comparisons of diversification rates suggest that genome doubling may have led to a dramatic increase in species richness in several angiosperm lineages, including Poaceae, Solanaceae, Fabaceae, and Brassicaceae. However, additional genomic studies are needed to pinpoint the exact phylogenetic placement of the ancient polyploidy events within these lineages and to determine when novel genes resulting from polyploidy have enabled adaptive radiations.     

Ancient lakes revisited: from the ecology to the genetics of speciation

Explosive speciation in ancient lakes has fascinated biologists for centuries and has inspired classical work on the tempo and modes of speciation. Considerable attention has been directed towards the extrinsic forces of speciation—the geological, geographical and ecological peculiarities of ancient lakes. Recently, there has been a resurgence of interest in the intrinsic nature of these radiations, the biological characteristics conducive to speciation. While new species are thought to arise mainly by the gradual enhancement of reproductive isolation among geographically isolated populations, ancient lakes provide little evidence for a predominant role of geography in speciation. Recent phylogenetic work provides strong evidence that multiple colonization waves were followed by parallel intralacustrine radiations that proceeded at relatively rapid rates despite long‐term gene flow through hybridization and introgression. Several studies suggest that hybridization itself might act as a key evolutionary mechanism by triggering major genomic reorganization/revolution and enabling the colonization of new ecological niches in ancient lakes. These studies propose that hybridization is not only of little impediment to diversification but could act as an important force in facilitating habitat transitions, promoting postcolonization adaptations and accelerating diversification. Emerging ecological genomic approaches are beginning to shed light on the long‐standing evolutionary dilemma of speciation in the face of gene flow. We propose an integrative programme for future studies on speciation in ancient lakes.     

THE CHALLENGE OF SPECIES DELIMITATION AT THE EXTREMES: DIVERSIFICATION WITHOUT MORPHOLOGICAL CHANGE IN PHILIPPINE SUN SKINKS

An accurate understanding of species diversity is essential to studies across a wide range of biological subdisciplines. However, delimiting species remains challenging in evolutionary radiations where morphological diversification is rapid and accompanied by little genetic differentiation or when genetic lineage divergence is not accompanied by morphological change. We investigate the utility of a variety of recently developed approaches to examine genetic and morphological diversity, and delimit species in a morphologically conserved group of Southeast Asian lizards. We find that species diversity is vastly underestimated in this unique evolutionary radiation, and find an extreme case where extensive genetic divergence among lineages has been accompanied by little to no differentiation in external morphology. Although we note that different conclusions can be drawn when species are delimited using molecular phylogenetics, coalescent‐based methods, or morphological data, it is clear that the use of a pluralistic approach leads to a more comprehensive appraisal of biodiversity, and greater appreciation for processes of diversification in this biologically important geographic region. Similarly, our approach demonstrates how recently developed methodologies can be used to obtain robust estimates of species limits in “nonadaptive” or “cryptic” evolutionary radiations.     

EXPLOSIVE RADIATION OR CRYPTIC MASS EXTINCTION? INTERPRETING SIGNATURES IN MOLECULAR PHYLOGENIES

How biodiversity is generated and maintained underlies many major questions in evolutionary biology, particularly relating to the tempo and pattern of diversification through time. Molecular phylogenies and new analytical methods provide additional tools to help interpret evolutionary processes. Evolutionary rates in lineages sometimes appear punctuated, and such "explosive" radiations are commonly interpreted as adaptive, leading to causative key innovations being sought. Here we argue that an alternative process might explain apparently rapid radiations ("broom-and-handle" or "stemmy" patterns seen in many phylogenies) with no need to invoke dramatic increase in the rate of diversification. We use simulations to show that mass extinction events can produce the same phylogenetic pattern as that currently being interpreted as due to an adaptive radiation. By comparing simulated and empirical phylogenies of Australian and southern African legumes, we find evidence for coincident mass extinctions in multiple lineages that could have resulted from global climate change at the end of the Eocene.     

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.     

Role of ancient lakes in genetic and phenotypic diversification of freshwater snails

Endemic organisms of ancient lakes have been studied as models to understand processes of speciation and adaptive radiation. However, it remains unclear how ancient lakes play roles in genetic and phenotypic diversity of freshwater mollusks. In the present study, we focus on viviparid freshwater snails in the ancient lakes of East and Southeast Asia (Japan and China) to address this question. Using molecular phylogenetic analyses based on mitochondrial (COI, 16S) and nuclear genes (18S, 28S, H3), we show that patterns of species diversification in viviparid lineages. Colonization to ancient lakes occurred independently in China and Japan at least four times, with subsequent diversification into more than two species within each lake group. Morphological analyses of fossil related viviparids suggest parallel phenotypic evolution occurred in the different lakes and ages. Each lake contained a single lineage which was phenotypically diversified relative to those from other sites. Using genome‐wide SNPs obtained by MIG‐seq, we also examined the genetic structure of three Japanese viviparids, including two endemic species of ancient Lake Biwa. The results suggest that these two species diversified from the population of the third species living in wetlands surrounding the lake. These findings suggest that rapid diversification of lineages and phenotypic divergence can occur in ancient lakes compared to other habitats. Formation of large lakes probably promotes speciation and phenotypic divergence as a result of adaptation into different microhabitats. High numbers of ancient lakes could be a driver of species diversity in Asian viviparid snails.     

Phylogenetic structure of mammal assemblages at large geographical scales: linking phylogenetic community ecology with macroecology

Phylogenetic community ecology seeks to explain the processes involved in the formation of species assemblages by analysing their phylogenetic structure, and to date has focused primarily on local-scale communities. Macroecology, on the other hand, is concerned with the structure of assemblages at large geographical scales, but has remained largely non-phylogenetic. Analysing the phylogenetic structure of large-scale assemblages provides a link between these two research programmes. In this paper, I ask whether we should expect large-scale assemblages to show significant phylogenetic structure, by outlining some of the ecological and macroevolutionary processes that may play a role in assemblage formation. As a case study, I then explore the phylogenetic structure of carnivore assemblages within the terrestrial ecoregions of Africa. Many assemblages at these scales are indeed phylogenetically non-random (either clustered or overdispersed). One interpretation of the observed patterns of phylogenetic structure is that many clades underwent rapid biome-filling radiations, followed by diversification slowdown and competitive sorting as niche space became saturated.