Evolutionary stasis and lability in thermal physiology in a group of tropical lizards

Understanding how quickly physiological traits evolve is a topic of great interest, particularly in the context of how organisms can adapt in response to climate warming. Adjustment to novel thermal habitats may occur either through behavioural adjustments, physiological adaptation or both. Here, we test whether rates of evolution differ among physiological traits in the cybotoids, a clade of tropical Anolis lizards distributed in markedly different thermal environments on the Caribbean island of Hispaniola. We find that cold tolerance evolves considerably faster than heat tolerance, a difference that results because behavioural thermoregulation more effectively shields these organisms from selection on upper than lower temperature tolerances. Specifically, because lizards in very different environments behaviourally thermoregulate during the day to similar body temperatures, divergent selection on body temperature and heat tolerance is precluded, whereas night-time temperatures can only be partially buffered by behaviour, thereby exposing organisms to selection on cold tolerance. We discuss how exposure to selection on physiology influences divergence among tropical organisms and its implications for adaptive evolutionary response to climate warming.     

Testing the island effect in adaptive radiation: rates and patterns of morphological diversification in Caribbean and mainland Anolis lizards

Many of the classic examples of adaptive radiation, including Caribbean Anolis lizards, are found on islands. However, Anolis also exhibits substantial species richness and ecomorphological disparity on mainland Central and South America. We compared patterns and rates of morphological evolution to investigate whether, in fact, island Anolis are exceptionally diverse relative to their mainland counterparts. Quite the contrary, we found that rates and extent of diversification were comparable--Anolis adaptive radiation is not an island phenomenon. However, mainland and Caribbean anoles occupy different parts of morphological space; in independent colonizations of both island and mainland habitats, island anoles have evolved shorter limbs and better-developed toe pads. These patterns suggest that the two areas are on different evolutionary trajectories. The ecological causes of these differences are unknown, but may relate to differences in predation or competition among mainland and island communities.     

Adaptive radiation and ecological opportunity in Sulawesi and Philippine fanged frog (Limnonectes) communities

Because island communities are derived from mainland communities, they are often less diverse by comparison. However, reduced complexity of island communities can also present ecological opportunities. For example, amphibian diversity on Sulawesi Island is lower than it is in the Philippines, but Sulawesi supports a surprising diversity of Sulawesi fanged frogs (Limnonectes). Here we examine molecular, morphological, and geographical variation of fanged frogs from these two regions. Using genealogical concordance, morphology, and a Bayesian approach to species delimitation, we identified 13 species on Sulawesi, only four of which have been previously described. After evolutionary history is accounted for, a model with multiple body size optima in sympatric species is favored over a "random-walk" model of body size evolution. Additionally, morphological variation is higher among sympatric than nonsympatric species on Sulawesi but not in the Philippines. These findings suggest that adaptive radiation of fanged frogs on Sulawesi was driven by natural selection to infiltrate ecological niches occupied by other frog lineages in the Philippines. This supports a role of ecological opportunity in community assembly: diversification in mature communities, such as the Philippines, is limited by a dearth of unoccupied ecological niches. On Sulawesi, evolutionary novelties originated in a predictable and replicated fashion in response to opportunities presented by a depauperate ancestral community.     

Mammals evolve faster on smaller islands

Island mammals often display remarkable evolutionary changes in size and morphology. Both theory and empirical data support the hypothesis that island mammals evolve at faster rates than their mainland congeners. It is also often assumed that the island effect is stronger and that evolution is faster on the smallest islands. I used a dataset assembled from the literature to test these assumptions for the first time. I show that mammals on smaller islands do indeed evolve more rapidly than mammals on larger islands, and also evolve by a greater amount. These results fit well the theory of an evolutionary burst due to the opening of new ecological opportunities on islands. This evolutionary burst is expected to be the strongest on the smallest islands where the contrast between the island and the mainland environments is the most dramatic.     

Ancient DNA Suggests Single Colonization and Within-Archipelago Diversification of Caribbean Caviomorph Rodents

Reconstructing the evolutionary history of island biotas is complicated by unusual morphological evolution in insular environments. However, past human-caused extinctions limit the use of molecular analyses to determine origins and affinities of enigmatic island taxa. The Caribbean formerly contained a morphologically diverse assemblage of caviomorph rodents (33 species in 19 genera), ranging from ∼0.1 to 200 kg and traditionally classified into three higher-order taxa (Capromyidae/Capromyinae, Heteropsomyinae, and Heptaxodontidae). Few species survive today, and the evolutionary affinities of living and extinct Caribbean caviomorphs to each other and to mainland taxa are unclear: Are they monophyletic, polyphyletic, or paraphyletic? We use ancient DNA techniques to present the first genetic data for extinct heteropsomyines and heptaxodontids, as well as for several extinct capromyids, and demonstrate through analysis of mitogenomic and nuclear data sets that all sampled Caribbean caviomorphs represent a well-supported monophyletic group. The remarkable morphological and ecological variation observed across living and extinct caviomorphs from Cuba, Hispaniola, Jamaica, Puerto Rico, and other islands was generated through within-archipelago evolutionary radiation following a single Early Miocene overwater colonization. This evolutionary pattern contrasts with the origination of diversity in many other Caribbean groups. All living and extinct Caribbean caviomorphs comprise a single biologically remarkable subfamily (Capromyinae) within the morphologically conservative living Neotropical family Echimyidae. Caribbean caviomorphs represent an important new example of insular mammalian adaptive radiation, where taxa retaining “ancestral-type” characteristics coexisted alongside taxa occupying novel island niches. Diversification was associated with the greatest insular body mass increase recorded in rodents and possibly the greatest for any mammal lineage.     

海洋岛屿生物多样性保育研究进展

海洋岛屿生态系统因具有明显的海域地理隔离而区别于陆地生态系统,被誉为生物地理与进化生态学研究的"天然实验室".陆地或其它邻近岛屿的种源物种迁移到新的岛屿后,经历地理隔离、特征置换或适应辐射等一系列的岛屿进化过程,形成与种源物种具有显著遗传差异的岛屿特有种.岛屿在小面积范围内分化形成大量的特有种,是岛屿生物多样性最为重要的特点之一.但是,岛屿种群由于分布范围局限、生境脆弱且种群规模较小,岛屿种群较陆地种群具有更高的灭绝风险.本文通过对海洋岛屿物种的起源与演化、遗传结构以及岛屿物种的濒危与保护3个热点问题的讨论,阐述岛屿生物多样性的形成机制、濒危肇因以及岛屿生物多样性保育的重要性.     

Genomic and phenomic analysis of island ant community assembly

Island biodiversity has long fascinated biologists as it typically presents tractable systems for unpicking the eco‐evolutionary processes driving community assembly. In general, two recurring themes are of central theoretical interest. First, immigration, diversification, and extinction typically depend on island geographical properties (e.g., area, isolation, and age). Second, predictable ecological and evolutionary trajectories readily occur after colonization, such as the evolution of adaptive trait syndromes, trends toward specialization, adaptive radiation, and eventual ecological decline. Hypotheses such as the taxon cycle draw on several of these themes to posit particular constraints on colonization and subsequent eco‐evolutionary dynamics. However, it has been challenging to examine these integrated dynamics with traditional methods. Here, we combine phylogenomics, population genomics and phenomics, to unravel community assembly dynamics among Pheidole (Hymenoptera, Formicidae) ants in the isolated Fijian archipelago. We uphold basic island biogeographic predictions that isolated islands accumulate diversity primarily through in situ evolution rather than dispersal, and population genomic support for taxon cycle predictions that endemic species have decreased dispersal ability and demography relative to regionally widespread taxa. However, rather than trending toward island syndromes, ecomorphological diversification in Fiji was intense, filling much of the genus‐level global morphospace. Furthermore, while most endemic species exhibit demographic decline and reduced dispersal, we show that the archipelago is not an evolutionary dead‐end. Rather, several endemic species show signatures of population and range expansion, including a successful colonization to the Cook islands. These results shed light on the processes shaping island biotas and refine our understanding of island biogeographic theory.     

The cryptic origins of evolutionary novelty: 1000‐fold faster trophic diversification rates without increased ecological opportunity or hybrid swarm

Ecological opportunity is frequently proposed as the sole ingredient for adaptive radiation into novel niches. An additional trigger may be genome‐wide hybridization resulting from “hybrid swarm.” However, these hypotheses have been difficult to test due to the rarity of comparable control environments lacking adaptive radiations. Here I exploit such a pattern in microendemic radiations of Caribbean pupfishes. I show that a sympatric three species radiation on San Salvador Island, Bahamas diversified 1445 times faster than neighboring islands in jaw length due to the evolution of a novel scale‐eating adaptive zone from a generalist ancestral niche. I then sampled 22 generalist populations on seven neighboring islands and measured morphological diversity, stomach content diversity, dietary isotopic diversity, genetic diversity, lake/island areas, macroalgae richness, and Caribbean‐wide patterns of gene flow. None of these standard metrics of ecological opportunity or gene flow were associated with adaptive radiation, except for slight increases in macroalgae richness. Thus, exceptional trophic diversification is highly localized despite myriad generalist populations in comparable environmental and genetic backgrounds. This study provides a strong counterexample to the ecological and hybrid swarm theories of adaptive radiation and suggests that diversification of novel specialists on a sparse fitness landscape is constrained by more than ecological opportunity and gene flow.     

Factors driving adaptive radiation in plants of oceanic islands: a case study from the Juan Fernández Archipelago

Adaptive radiation is a common evolutionary phenomenon in oceanic islands. From one successful immigrant population, dispersal into different island environments and directional selection can rapidly yield a series of morphologically distinct species, each adapted to its own particular environment. Not all island immigrants, however, follow this evolutionary pathway. Others successfully arrive and establish viable populations, but they remain in the same ecological zone and only slowly diverge over millions of years. This transformational speciation, or anagenesis, is also common in oceanic archipelagos. The critical question is why do some groups radiate adaptively and others not? The Juan Fernández Islands contain 105 endemic taxa of angiosperms, 49% of which have originated by adaptive radiation (cladogenesis) and 51% by anagenesis, hence providing an opportunity to examine characteristics of taxa that have undergone both types of speciation in the same general island environment. Life form, dispersal mode, and total number of species in progenitors (genera) of endemic angiosperms in the archipelago were investigated from literature sources and compared with modes of speciation (cladogenesis vs. anagenesis). It is suggested that immigrants tending to undergo adaptive radiation are herbaceous perennial herbs, with leaky self-incompatible breeding systems, good intra-island dispersal capabilities, and flexible structural and physiological systems. Perhaps more importantly, the progenitors of adaptively radiated groups in islands are those that have already been successful in adaptations to different environments in source areas, and which have also undergone eco-geographic speciation. Evolutionary success via adaptive radiation in oceanic islands, therefore, is less a novel feature of island lineages but rather a continuation of tendency for successful adaptive speciation in lineages of continental source regions.     

Convergence in reduced body size,head size,and blood glucose in three island reptiles

Many oceanic islands harbor diverse species that differ markedly from their mainland relatives with respect to morphology, behavior, and physiology. A particularly common morphological change exhibited by a wide range of species on islands worldwide involves either a reduction in body size, termed island dwarfism, or an increase in body size, termed island gigantism. While numerous instances of dwarfism and gigantism have been well documented, documentation of other morphological changes on islands remains limited. Furthermore, we lack a basic understanding of the physiological mechanisms that underlie these changes, and whether they are convergent. A major hypothesis for the repeated evolution of dwarfism posits selection for smaller, more efficient body sizes in the context of low resource availability. Under this hypothesis, we would expect the physiological mechanisms known to be downregulated in model organisms exhibiting small body sizes due to dietary restriction or artificial selection would also be downregulated in wild species exhibiting dwarfism on islands. We measured body size, relative head size, and circulating blood glucose in three species of reptiles—two snakes and one lizard—in the California Channel Islands relative to mainland populations. Collating data from 6 years of study, we found that relative to mainland population the island populations had smaller body size (i.e., island dwarfism), smaller head sizes relative to body size, and lower levels of blood glucose, although with some variation by sex and year. These findings suggest that the island populations of these three species have independently evolved convergent physiological changes (lower glucose set point) corresponding to convergent changes in morphology that are consistent with a scenario of reduced resource availability and/or changes in prey size on the islands. This provides a powerful system to further investigate ecological, physiological, and genetic variables to elucidate the mechanisms underlying convergent changes in life history on islands.     

Ecological specialization and morphological diversification in Greater Antillean boas

Colonization of islands can dramatically influence the evolutionary trajectories of organisms, with both deterministic and stochastic processes driving adaptation and diversification. Some island colonists evolve extremely large or small body sizes, presumably in response to unique ecological circumstances present on islands. One example of this phenomenon, the Greater Antillean boas, includes both small (<90 cm) and large (4 m) species occurring on the Greater Antilles and Bahamas, with some islands supporting pairs or trios of body‐size divergent species. These boas have been shown to comprise a monophyletic radiation arising from a Miocene dispersal event to the Greater Antilles, though it is not known whether co‐occurrence of small and large species is a result of dispersal or in situ evolution. Here, we provide the first comprehensive species phylogeny for this clade combined with morphometric and ecological data to show that small body size evolved repeatedly on separate islands in association with specialization in substrate use. Our results further suggest that microhabitat specialization is linked to increased rates of head shape diversification among specialists. Our findings show that ecological specialization following island colonization promotes morphological diversity through deterministic body size evolution and cranial morphological diversification that is contingent on island‐ and species‐specific factors.     

Key innovations and island colonization as engines of evolutionary diversification: a comparative test with the Australasian diplodactyloid geckos

The acquisition of key innovations and the invasion of new areas constitute two major processes that facilitate ecological opportunity and subsequent evolutionary diversification. Using a major lizard radiation as a model, the Australasian diplodactyloid geckos, we explored the effects of two key innovations (adhesive toepads and a snake‐like phenotype) and the invasion of new environments (island colonization) in promoting the evolution of phenotypic and species diversity. We found no evidence that toepads had significantly increased evolutionary diversification, which challenges the common assumption that the evolution of toepads has been responsible for the extensive radiation of geckos. In contrast, a snakelike phenotype was associated with increased rates of body size evolution and, to a lesser extent, species diversification. However, the clearest impact on evolutionary diversification has been the colonization of New Zealand and New Caledonia, which were associated with increased rates of both body size evolution and species diversification. This highlights that colonizing new environments can drive adaptive diversification in conjunction or independently of the evolution of a key innovation. Studies wishing to confirm the putative link between a key innovation and subsequent evolutionary diversification must therefore show that it has been the acquisition of an innovation specifically, not the colonization of new areas more generally, that has prompted diversification.     

Rapid parallel evolution of aberrant traits in the diversification of the Gulf of Guinea white-eyes (Aves, Zosteropidae)

Archipelago-endemic bird radiations are familiar to evolutionary biologists as key illustrations of evolutionary patterns. However, such radiations are in fact rare events. White-eyes (Zosteropidae) are birds with an exceptionally high colonization and speciation potential; they have colonized more islands globally than any other passerine group and include the most species-rich bird genus. The multiplication of white-eye island endemics has been consistently attributed to independent colonizations from the mainland; the white-eyes of the Gulf of Guinea archipelago had been seen as a classic case, spanning as great a breadth of phenotypic diversity as the family worldwide. Contrary to this hypothesis, our molecular phylogenetic analysis places the Gulf of Guinea white-eyes in just two radiations, one grouping all five oceanic island taxa and the other grouping continental island and land-bridge taxa. Numerous 'aberrant' phenotypes (traditionally grouped in the genus Speirops) have evolved independently over a short space of time from nonaberrant (Zosterops) phenotypes; the most phenotypically divergent species have separated as recently as 0.22 Ma. These radiations rival those of Darwin's finches and the Hawaiian honeycreepers in terms of the extent of adaptive radiation per unit time, both in terms of species numbers and in terms of phenotypic diversity. Tempo and patterns of morphological divergence are strongly supportive of an adaptive radiation in the oceanic islands driven by ecological interactions between sympatric white-eyes. Here, very rapid phenotypic evolution mainly affected taxa derived from the youngest wave of colonization, in accordance with the model of asymmetric divergence owing to resource competition in sympatry.     

Genetic and phylogenetic consequences of island biogeography

Abstract.— Island biogeography theory predicts that the number of species on an island should increase with island size and decrease with island distance to the mainland. These predictions are generally well supported in comparative and experimental studies. These ecological, equilibrium predictions arise as a result of colonization and extinction processes. Because colonization and extinction are also important processes in evolution, we develop methods to test evolutionary predictions of island biogeography. We derive a population genetic model of island biogeography that incorporates island colonization, migration of individuals from the mainland, and extinction of island populations. The model provides a means of estimating the rates of migration and extinction from population genetic data. This model predicts that within an island population the distribution of genetic divergences with respect to the mainland source population should be bimodal, with much of the divergence dating to the colonization event. Across islands, this model predicts that populations on large islands should be on average more genetically divergent from mainland source populations than those on small islands. Likewise, populations on distant islands should be more divergent than those on close islands. Published observations of a larger proportion of endemic species on large and distant islands support these predictions.     

Dwarfism in insular sloths: biogeography,selection, and evolutionary rate

The islands of Bocas del Toro, Panama, were sequentially separated from the adjacent mainland by rising sea levels during the past 10,000 years. Three-toed sloths (Bradypus) from five islands are smaller than their mainland counterparts, and the insular populations themselves vary in mean body size. We first examine relationships between body size and physical characteristics of the islands, testing hypotheses regarding optimal body size, evolutionary equilibria, and the presence of dispersal in this system. To do so, we conduct linear regressions of body size onto island area, distance from the mainland, and island age. Second, we retroactively calculate two measures of the evolutionary rate of change in body size (haldanes and darwins) and the standardized linear selection differential, or selection intensity (i). We also test the observed morphological changes against models of evolution by genetic drift. The results indicate that mean body size decreases linearly with island age, explaining up to 97% of the variation among population means. Neither island area nor distance from the mainland is significant in multiple regressions that include island age. Thus, we find no evidence for differential optimal body size among islands, or for dispersal in the system. In contrast, the dependence of body size on island age suggests uniform directional selection for small body size in the insular populations. Although genetic drift cannot be discounted as the cause for this evolution in body size, the probability is small given the consistent direction of evolution (repeated dwarfism). The insular sloths show a sustained rate of evolution similar to those measured in haldanes over tens of generations, appearing to unite micro- and macroevolutionary time scales. Furthermore, the magnitude and rate of this example of rapid differentiation fall within predictions of theoretical models from population genetics. However, the linearity of the relationship between body size and island age is not predicted, suggesting that either more factors are involved than those considered here, or that theoretical advances are necessary to explain constant evolutionary rates over long time spans in new selective environments.     

Out of Hawaii: the origin and biogeography of the genus Scaptomyza (Diptera: Drosophilidae)

The Hawaiian Archipelago is the most isolated island system on the planet and has been the subject of evolutionary research for over a century. The largest radiation of species in Hawaii is the Hawaiian Drosophilidae, a group of approximately 1000 species. Dispersal to isolated island systems like Hawaii is rare and the resultant flora and fauna shows high disharmony with mainland communities. The possibility that some lineages may have originated in Hawaii and subsequently 'escaped' to diversify on continental landmasses is expected to be rarer still. We present phylogenetic analysis of 134 partially sequenced mitochondrial genomes of Drosophilidae (approx. 1.3 Mb of sequence total) to address major aspects of adaptive radiation and dispersal in Hawaii. We show that the genus Scaptomyza, a group that accounts for approximately one-third of the species-level diversity of Drosophilidae in the Hawaiian Islands, originated in Hawaii, diversified there, and subsequently colonized a number of island and continental landmasses elsewhere on the globe. We propose that a combination of small body size, rapid generation time and unique ecological and physiological adaptations have allowed this genus to effectively disperse and diversify.     

Are island and mainland biotas different? Richness and level of generalism in parasitoids of a microlepidopteran in Macaronesia

Island communities are exposed to several evolutionary and ecological processes that lead to changes in their diversity and structure compared to mainland biotas. These phenomena have been observed for various taxa but not for parasitoids, a key group in terms of community diversity and functioning. Here we use the parasitoid communities associated with the moth Acroclita subsequana (Lepidoptera: Tortricidae) in the Macaronesian region, to test whether species richness differs between islands and mainland, and whether island parasitoid faunas are biased towards generalist species. Host larvae were collected on several islands and adjacent mainland, carefully searched for ectoparasitoid larvae and dissected to recover any endoparasitoids. Parasitoids were classified as idiobionts, which usually have a wide host range (i.e. generalists), or koinobionts that are considered specialists. Mainland species richness was lower than expected by chance, with most of the species being koinobionts. On the other hand, island communities showed a greater proportion of idiobiont species. Overall parasitism rates were similar between islands and mainland, but islands had higher rates of parasitism by idiobionts than expected by chance, and mainland areas showed the highest koinobiont parasitism rates. These results suggest that island parasitoid communities are dominated by generalists, in comparison to mainland communities. Several hypotheses may explain this pattern: (1) generalist parasitoids might have better dispersal abilities; (2) they may be less constrained by ‘sequential dependencies’; and (3) island parasitoids probably have fewer competitors and/or predators, thus favouring the establishment of generalists. New studies including multiple hosts, other habitats, and/or more islands are necessary to identify which of these processes shape island parasitoid communities.     

The impact of insularity on the thermoregulation of a Mediterranean lizard

The overall biology of ectotherms is strongly affected by the thermal quality of the environment. The particular conditions prevailing on islands have a strong effect on numerous features of animal life. In this study we compared mainland and island populations of the lizard Lacerta trilineata and hypothesized that insularity would affect the thermoregulatory strategy. Continental habitats were of lower thermal quality, experiencing more intense fluctuations and had higher values of operative temperatures. Nevertheless mainland lizards selected for higher body temperatures in the lab and showed more effective thermoregulation during summer than their island peers. Lizards achieved similar body temperatures in the field in both types of habitat, underlining the importance of predation as a potential factor to mainland lizards that failed to reach their higher thermal preferences. Both island and mainland populations of L. trilineata have been adapted to their thermal environment, supporting the labile view on the evolution of thermal physiology for this species.     

Dimorphism and divergence in island and mainland Anoles

Relative to the West Indies, the ecology and evolution of anoles inhabiting islands off Central and South America have received little attention. The paucity of studies on continental islands has limited our ability to generalize and extend results based on the West Indian paradigm, as well as our understanding of the profound differences between the adaptive radiations of continental vs. Greater Antillean anoles. Here we compare the morphological, ecological, behavioural and genetic divergence between Anolis nebulosus populations inhabiting a small island in the Bay of Chamela, Mexico, and a nearby mainland forest. Notably, the two populations exhibit intra‐sexual dimorphism with respect to head and limb sizes, the first such polymorphism documented for an Anolis species. We also compare the shape of island and mainland A. nebulosus with each other, the six West Indian ecomorphs and a hypothetical generalist species. Finally, we address the generalist convergence hypothesis for anoles on single species islands. We conclude that convergence on a generalist morphology is widespread among solitary anoles in the West Indies. We present data on a limited sample of solitary anoles with mainland ancestors that suggest a parallel convergence on a similar generalist morphology, probably due to similar adaptive landscapes shaped by selective forces common to small island environments.     

BODY SIZE DIVERSIFICATION IN ANOLIS: NOVEL ENVIRONMENT AND ISLAND EFFECTS

Extreme morphologies of many insular taxa suggest that islands have unusual properties that influence the tempo and mode of evolution. Yet whether insularity per se promotes rapid phenotypic evolution remains largely untested. We extend a phylogenetic comparative approach to test the influence of novel environments versus insularity on rates of body size and sexual size dimorphism diversification in Anolis . Rates of body size diversification among small-island and mainland species were similar to those of anole species on the Greater Antilles. However, the Greater Antilles taxa that colonized small islands and the mainland are ecologically nonrandom: rates of body size diversification among small-island and mainland species are high compared to their large-island sister taxa. Furthermore, rates of diversification in sexual size dimorphism on small islands are high compared to all large-island and mainland lineages. We suggest that elevated diversifying selection, particularly as a result of ecological release, may drive high rates of body size diversification in both small-island and mainland novel environments. In contrast, high abundance (prevalent among small-island lizard communities) mediating intraspecific resource competition and male–male competition may explain why sexual size dimorphism diversifies faster among small-island lineages than among their mainland and large-island relatives.