Evolutionary assembly of island faunas reverses the classic island–mainland richness difference in Anolis lizards

Aim Islands are widely considered to be species depauperate relative to mainlands but, somewhat paradoxically, are also host to many striking adaptive radiations. Here, focusing on Anolis lizards, we investigate if cladogenetic processes can reconcile these observations by determining if in situ speciation can reduce, or even reverse, the classical island–mainland richness discrepancy. Location Caribbean islands and the Neotropical mainland. Methods We constructed range maps for 203 mainland anoles from museum records and evaluated whether geographical area could account for differences in species richness between island and mainland anole faunas. We compared the island species–area relationship with total mainland anole diversity and with the richness of island‐sized mainland areas. We evaluated the role of climate in the observed differences by using Bayesian model averaging to predict island richness based on the mainland climate–richness relationship. Lastly, we used a published phylogeny and stochastic mapping of ancestral states to determine if speciation rate was greater on islands, after accounting for differences in geographical area. Results Islands dominated by in situ speciation had, on average, significantly more species than similarly sized mainland regions, but islands where in situ speciation has not occurred were species depauperate relative to mainland areas. Results were similar at the scale of the entire mainland, although marginally non‐significant. These findings held even after accounting for climate. Speciation has not been faster on islands; instead, when extinction was assumed to be low, speciation rate varied consistently with geographical area. When extinction was high, there was some evidence that mainland speciation was faster than expected based on area. Main conclusions Our results indicate that evolutionary assembly of island faunas can reverse the general pattern of reduced species richness on islands relative to mainlands.     

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     

Physiological evolution during adaptive radiation: A test of the island effect in Anolis lizards

Phenotypic evolution is often exceptionally rapid on islands, resulting in numerous, ecologically diverse species. Although adaptive radiation proceeds along various phenotypic axes, the island effect of faster evolution has been mostly tested with regard to morphology. Here, we leveraged the physiological diversity and species richness of Anolis lizards to examine the evolutionary dynamics of three key traits: heat tolerance, body temperature, and cold tolerance. Contrary to expectation, we discovered slower heat tolerance evolution on islands. Additionally, island species evolve toward higher optimal body temperatures than mainland species. Higher optima and slower evolution in upper physiological limits are consistent with the Bogert effect, or evolutionary inertia due to thermoregulation. Correspondingly, body temperature is higher and more stable on islands than on the American mainland, despite similarity in thermal environments. Greater thermoregulation on islands may occur due to ecological release from competitors and predators compared to mainland environments. By reducing the costs of thermoregulation, ecological opportunity on islands may actually stymie, rather than hasten, physiological evolution. Our results emphasize that physiological diversity is an important axis of ecological differentiation in the adaptive radiation of anoles, and that behavior can impart distinct macroevolutionary footprints on physiological diversity on islands and continents.     

Patterns of ecomorphological convergence among mainland and island Anolis lizards

Differing selective pressures on islands versus the mainland may produce alternative evolutionary outcomes among closely related lineages. Conversely, lineages may be constrained to produce similar outcomes in different mainland and island environments, or mainland and island environments may not differ significantly. Among the best‐studied island radiations are Caribbean Anolis lizards. Distinct morphotypes, or ‘ecomorphs’, have been described, and the same ecomorphs have evolved independently on each Greater Antillean island. The mainland Anolis radiation has received much less attention. We use a large morphological data set and a novel phylogenetic hypothesis to show that mainland Anolis did not evolve the same morphotypes as island Anolis, despite some island species being more closely related to mainland species than to island species that share their morphotype. A maximum of four of the six Caribbean ecomorphs were found to exist on the mainland, and just 15 of 123 mainland species are assignable to a Caribbean ecomorph. This result was insensitive to differing taxon samples and alternative phylogenetic hypotheses. Mainland convergence to a Caribbean ecomorph occurs only among species assigned to the grass‐bush ecomorph. Thus, the ecomorphs that have evolved convergently multiple times in the Caribbean have not evolved in parallel on the mainland. These results are consistent with the hypothesis that mainland and island environments offer different selective pressures. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 852–859.     

Adaptive radiation versus intraspecific differentiation: morphological variation in Caribbean Anolis lizards

Lizards in the genus Anolis have experienced adaptive radiation in the Greater Antilles, producing a suite of species morphologically adapted to use different parts of the environment. In the Lesser Antilles, adaptive radiation has not occurred, but on some islands, interpopulational variation is high and represents adaptation to different habitats. We compared the extent of morphological differentiation among Greater Antillean habitat specialists with that exhibited among populations of two species, Anolis marmoratus and A. oculatus, from the Lesser Antillean islands of Guadeloupe and Dominica. Although extensive, intraspecific divergence in the Lesser Antilles is substantially less in magnitude than the differences among habitat specialists in the Greater Antilles. All populations of A. marmoratus are most similar to Greater Antillean trunk‐crown habitat specialists, but populations of A. oculatus differ in their affinities: some are similar to trunk‐crown anoles, but others are more similar to trunk‐ground habitat specialists.     

Testing for unequal rates of morphological diversification in the absence of a detailed phylogeny: a case study from Characiform fishes

This study develops the random phylogenies rate test (RAPRATE), a likelihood method that simulates morphological evolution along randomly generated phylogenies, and uses it to determine whether a considerable difference in morphological diversity between two sister clades of South American fishes should be taken as evidence of differing rates of morphological change or lineage turnover. Despite identical ages of origin, similar species richness, and sympatric geographic distributions, the morphological and ecological diversity of the superfamily Anostomoidea exceeds that of the Curimatoidea. The test shows with 90% confidence (using variance among species as the measure of morphological diversity) or 99% confidence (using volume of occupied morphospace) that the rate of morphological change per unit time in the Anostomoidea likely exceeded that of the Curimatoidea. Variation in the rate of lineage turnover (speciation and extinction rates) is not found to affect greatly the morphological diversity of simulated clades and is not a likely explanation of the observed difference in morphological diversity in this case study. Though a 17% or greater delay in the onset of diversification in the Curimatoidea remains a possible alternative explanation of unequal morphological diversification, further simulations suggest that two clades drawn from the possible treespace of the Anostomoidea and Curimatoidea will rarely differ so greatly in the onset of diversification. Several uniquely derived morphological and ecological features of the Anostomoidea and Curimatoidea may have accelerated or decelerated their rate of morphological change, including a marked lengthening of the quadrate that may have relaxed structural constraints on the evolution of the anostomoid jaw.     

Profile of a flower: How rates of morphological evolution drive floral diversification in Ericales and angiosperms

Premise

Recent studies of floral disparity in the asterid order Ericales have shown that flowers vary strongly among families and that disparity is unequally distributed between the three flower modules (perianth, androecium, gynoecium). However, it remains unknown whether these patterns are driven by heterogeneous rates of morphological evolution or other factors.

Methods

Here, we compiled a data set of 33 floral characters scored for 414 species of Ericales sampled from 346 genera and all 22 families. We conducted ancestral state reconstructions using an equal-rates Markov model for each character. We estimated rates of morphological evolution for Ericales and for a separate angiosperm-wide data set of 19 characters and 792 species, creating “rate profiles” for Ericales, angiosperms, and major angiosperm subclades. We compared morphological rates among flower modules within each data set separately and between data sets, and we compared rates among angiosperm subclades using the angiosperm data set.

Results

The androecium exhibits the highest evolutionary rates across most characters, whereas most perianth and gynoecium characters evolve more slowly in both Ericales and angiosperms. Both high and low rates of morphological evolution can result in high floral disparity in Ericales. Analyses of an angiosperm-wide floral data set reveal that this pattern appears to be conserved across most major angiosperm clades.

Conclusions

Elevated rates of morphological evolution in the androecium of Ericales may explain the higher disparity reported for this floral module. Comparing rates of morphological evolution through rate profiles proves to be a powerful tool in understanding floral evolution.     

Small island biogeography in the Gulf of California: lizards, the subsidized island biogeography hypothesis, and the small island effect

Aim We used insular lizard communities to test the predictions of two hypotheses that attempt to explain patterns of species richness on small islands. We first address the subsidized island biogeography (SIB) hypothesis, which predicts that spatial subsidies may cause insular species richness to deviate from species–area predictions, especially on small islands. Next, we examine the small island effect (SIE), which suggests small islands may not fit the traditional log‐linear species–area curve. Location Islands with arthropodivorous lizard communities throughout the Gulf of California. Methods To evaluate the SIB hypothesis, we first identified subsidized and unsubsidized islands based on surrogate measures of allochthonous productivity (i.e. island size and bird presence). Subsequently, we created species–area curves from previously published lizard species richness and island area data. We used the residuals and slopes from these analyses to compare species richness on subsidized and unsubsidized islands. To test for an SIE, we used breakpoint regression to model the relationship between lizard species richness and island area. We compared results from this model to results from the log‐linear regression model. Results Subsidized islands had a lower slope than unsubsidized islands, and the difference between these groups was significant when small islands were defined as < 1 km². In addition to comparing slopes, we tested for differences in the magnitude of the residuals (from the species–area regression of all islands) for subsidized vs. unsubsidized islands. We found no significant patterns in the residual values for small vs. large islands, or between islands with and without seabirds. The SIE was found to be a slightly better predictor of lizard species richness than the traditional log‐linear model. Main conclusions Predictions of the SIB hypothesis were partially supported by the data. The absence of a significant SIE may be a result of spatial subsidies as explained by the SIB hypothesis and data presented here. We conclude by suggesting potential scenarios to test for interactions between these two small island hypotheses. Future studies considering factors affecting species richness should examine the possible role of spatial subsidies, an SIE, or a synergistic effect of the two in data sets with small islands.     

Ancient and contingent body shape diversification in a hyperdiverse continental fish radiation

The characiform fishes of the Neotropics and Africa radiated remarkably in ecomorphology, but the macroevolutionary processes responsible for their biodiversity remain unexplored, and the degree to which their continental diversification parallels classic adaptive radiations remains untested. We reconstruct their diversification using a new fossil‐calibrated molecular phylogeny, dietary information, and geometric morphometrics. Though body shape diversified early in a manner consistent with an ancient continental adaptive radiation, trophic shifts did not always coincide with shape changes. With the notable exception of piscivores, lineages that converged in diet did not converge closely in body shape. Shifts in habitat or other variables likely influenced body shape evolution in addition to changes in diet, and the clade's history departs from many classic adaptive radiations in lakes or on islands, in which trophic convergence drives morphological convergence. The contrast between the Neotropical radiation's exhaustive exploration of morphospace and the more restrained diversification in Africa suggests a major role for contingency in characiform evolution, with the presence of cypriniform competitors in the Old World, but not the New, providing one possible explanation. Our results depict the clearest ecomorphological reconstruction to date for Characiformes and set the stage for studies further elucidating the processes underlying its diversification.     

Convergent evolution of phenotypic integration and its alignment with morphological diversification in Caribbean Anolis ecomorphs

The adaptive landscape and the G-matrix are keys concepts for understanding how quantitative characters evolve during adaptive radiation. In particular, whether the adaptive landscape can drive convergence of phenotypic integration (i.e., the pattern of phenotypic variation and covariation summarized in the P-matrix) is not well studied. We estimated and compared P for 19 morphological traits in eight species of Caribbean Anolis lizards, finding that similarity in P among species was not correlated with phylogenetic distance. However, greater similarity in P among ecologically similar Anolis species (i.e., the trunk-ground ecomorph) suggests the role of convergent natural selection. Despite this convergence and relatively deep phylogenetic divergence, a large portion of eigenstructure of P is retained among our eight focal species. We also analyzed P as an approximation of G to test for correspondence with the pattern of phenotypic divergence in 21 Caribbean Anolis species. These patterns of covariation were coincident, suggesting that either genetic constraint has influenced the pattern of among-species divergence or, alternatively, that the adaptive landscape has influenced both G and the pattern of phenotypic divergence among species. We provide evidence for convergent evolution of phenotypic integration for one class of Anolis ecomorph, revealing yet another important dimension of evolutionary convergence in this group.     

Climatic niche evolution in Smilacaceae (Liliales) drives patterns of species diversification and richness between the Old and New World

Geographical variation in species richness in plant groups is determined by the interplay between historical, evolutionary, and ecological processes. However, the processes underlying the striking disparity in species richness between Asia and the Americas remain poorly understood. Here, we synthesize global phylogenetic and macroecological data on the diversification of Smilacaceae, deciphering potential drivers underlying the species diversity pattern biased toward Asia. We compiled global distributions of all Smilacaceae species, and reconstructed the biogeographic history and niche evolution using a new time-calibrated phylogeny (eight genes, 135 species). Integrating these data sets, we estimated evolutionary histories and diversification rates for each region, and tested correlations among species diversification, niche evolution, and niche divergence. Smilacaceae probably originated during the Late Cretaceous/Early Palaeocene and began to diversify in middle to low latitudes in Central America and Eurasia during the Late Eocene. Both the Old and New World clades exhibited a steady, albeit slight, increase of species diversification from the Late Eocene to Early Miocene. However, the Old World clade experienced an abrupt increase in net diversification during the Late Miocene. Our findings also revealed that species diversification rates were positively correlated with ecological niche evolution and niche divergence. Niche shifts and climatic niche evolution since the Middle Miocene played crucial roles in species diversification dynamics within Smilacaceae. The high plant richness in Asia may be explained by greater diversification in this region, potentially promoted by heterogeneous environments.     

Testing island biogeography theory with visitation rates of birds to British islands

Aim We consider three hypotheses – MacArthur and Wilson’s island biogeography theory (IBT), Lack’s habitat diversity idea and the ‘target effect’– that explain the pattern of decreased species richness on small and distant islands. Location We evaluate these hypotheses using a detailed dataset on the occurrence and abundance of terrestrial birds on nine islands off the coast of Britain and the Republic of Ireland. Methods  Unlike previous studies, we compile data on species that visit the islands, rather than just those that breed on them. We divided the species into five mutually exclusive categories based upon their migratory status and where they regularly breed: British residents, summer visitors to Britain, winter visitors to Britain, and vagrants from Europe or beyond Europe. For each species group on each island we calculated the average number of species visiting each year. We then regressed the average number of species against island area and distance to the mainland (all variables were log‐transformed). We also compared the average number of species visiting each island with the average number of species breeding on each island. Results  Average number of visiting British residents decreased significantly with increasing island distance, but showed no relationship with island area. There was no significant relationship between island area or island distance and average number of summer or winter visitors. European and non‐European vagrants likewise showed no relationship between numbers of species visiting and island distance. However, the relationship between island area and number of visiting species was significant for both these categories; as island area increases so too does the number of visiting species. Main conclusions  As predicted by IBT, there were fewer visiting species on more distant islands. There were substantially more visitors to each island than breeding species, supporting Lack’s argument that lower bird richness is not a result of varying immigration rates (as predicted by IBT) but rather a result of some other island property, e.g. fewer resources. Birds make a decision to either leave an island or stay and breed. The target effect was also clearly demonstrated by the increase in European and non‐European breeders with increasing island size.     

Comparative rates of lower jaw diversification in cichlid adaptive radiations

The lower jaw (LJ) provides an ideal trophic phenotype to compare rates and patterns of macroevolution among cichlid radiations. Using a novel phylogeny of four genes (ND2, dlx2, mitfb, and s7), we examined the evolutionary relationships among two of the most phylogenetically disparate cichlid radiations: (i) the Central America Heroines; and (ii) the East African Lake Malawi flock. To quantify jaw morphology, we measured two LJ lever systems in approximately 40 species from each lineage. Using geologic calibrations, we generated a chronogram for both groups and examined the rates of jaw evolution in the two radiations. The most rapidly evolving components of the LJ differed between the two radiations. However, the Lake Malawi flock exhibited a much faster rate of evolution in several components of the LJ. This rapid rate of divergence is consistent with natural selection, promoting unparalleled trophic diversification in Lake Malawi cichlids.     

Enemy at the gates: Rapid defensive trait diversification in an adaptive radiation of lizards

Adaptive radiation (AR), the product of rapid diversification of an ancestral species into novel adaptive zones, has become pivotal in our understanding of biodiversity. Although it has widely been accepted that predators may drive the process of AR by creating ecological opportunity (e.g., enemy‐free space), the role of predators as selective agents in defensive trait diversification remains controversial. Using phylogenetic comparative methods, we provide evidence for an “early burst” in the diversification of antipredator phenotypes in Cordylinae, a relatively small AR of morphologically diverse southern African lizards. The evolution of body armor appears to have been initially rapid, but slowed down over time, consistent with the ecological niche‐filling model. We suggest that the observed “early burst” pattern could be attributed to shifts in vulnerability to different types of predators (i.e., aerial versus terrestrial) associated with thermal habitat partitioning. These results provide empirical evidence supporting the hypothesis that predators or the interaction therewith might be key components of ecological opportunity, although the way in which predators influence morphological diversification requires further study.     

Taxic and morphological diversification during the early radiation of Clupeomorpha (Actinopterygii,Teleostei)

Evolutionary radiation is a problematic concept whose definition and classification have recently changed. Radiations can be defined as the pattern of abrupt increase in diversity of a lineage. It is relevant to evaluate the presence and interaction of different types of radiation in extant and fossil organisms to adequately delimitate the radiation types and to know the diversity in the context of Earth's history. Here, we employed the superorder Clupeomorpha at the Early–Late Cretaceous boundary as a study case to investigate radiation types and their interactions, using both taxic and morphological approaches. Clupeomorpha is an extensively studied, diverse and ancient teleostean superorder with wide geographical and ecological distributions. We propose a model for calculating rates of origination in order to analyse the taxic diversification and employ geometric morphometrics to analyse the morphological diversification that occurred at the temporal boundary. The results suggest the absence of taxic radiation due to a constant increase in taxon origination. However, the expansion of the phylomorphospace occupation and the disparity increase suggest the presence of a ‘climatic–geographical’ or ‘broad diversification-like’ disparity, according to current classifications. This illustrates the incompatibility of current radiation classifications with this case study.     

The influence of multiple functional demands on morphological diversification: A test on turtle shells

Organismal parts are often involved in the performance of more than one function. The role of trade‐offs in influencing phenotypic evolution of such parts is well‐studied; less well‐understood is their role in influencing phenotypic diversity. Increases in the number of functions a part is involved in may inhibit subsequent diversification, as the number of trade‐offs increases. Alternately, such an increase might promote phenotypic diversification, by increasing adaptive landscape complexity and promoting specialization for different roles. We compare these predictions by testing whether aquatic turtle shells, which resist loads, act as hydrodynamic elements, facilitate self‐righting, and exchange heat with the environment, differ in phenotypic diversity from those of terrestrial species, which perform all the same functions except for hydrodynamics. We used 53 3D landmarks digitized on 2722 specimens of 274 hard‐shelled turtle species to quantify shell shape variation, and a set of phylogenetic hypotheses to examine evolutionary patterns. Terrestrial turtles consistently had higher phenotypic diversity than aquatic species. Differences are not due to differences in the rates of evolution between the two groups, but rather differences in evolutionary mode. Thus this study supports the traditional view of the role of multiple functions in determining phenotypic diversity.     

Phenotypic integration between claw and toepad traits promotes microhabitat specialization in the Anolis adaptive radiation

The performance of an organism in its environment frequently depends more on its composite phenotype than on individual phenotypic traits. Thus, understanding environmental adaptation requires investigating patterns of covariation across functionally related traits. The replicated adaptive radiations of Greater Antillean Anolis lizards are characterized by ecological and morphological convergence, thus, providing an opportunity to examine the role of multiple phenotypes in microhabitat adaptation. Here, we examine integrated claw and toepad morphological evolution in relation to habitat partitioning across the adaptive radiations of Greater Antillean anoles. Based on analysis of 428 specimens from 57 species, we found that different aspects of claw morphology were associated with different perch dimensions, with claw height positively associated with perch diameter and claw curvature positively associated with perch height. Patterns of integration also varied across claw and toepad traits, likely driven by correlative selection for performance on smoother and rougher substrates. Finally, rates of evolution differed between claw and toepad traits, with claw length evolving faster than all other traits despite having no predicted functional importance. Our results highlight the multivariate nature of phenotypic adaptation and suggest that phenotypic integration across Greater Antillean anoles is driven by fine‐scale correlative selection based on structural habitat specialization.