Experimental studies of adaptive differentiation in Bahamian Anolis lizards

Populations of the lizards Anolis carolinensis and A. sagrei were experimentally introduced onto small islands in the Bahamas. Less than 15 years after introduction, we investigated whether the populations had diverged and, if so, whether differentiation was related to island vegetational characteristics or propagule size. No effect of founding population size was evident, but differentiation of A. sagrei appears to have been adaptive, a direct relationship existed between how vegetationally different an experimental island was from the source island and how much the experimental population on that island had diverged morphologically. Populations of A. carolinensis had also diverged, but were too few for quantitative comparisons. A parallel exists between the divergence of experimental populations of A. sagrei and the adaptive radiation of Anolis lizards in the Greater Antilles; in both cases, relative hindlimb length and perch diameter are strongly correlated. This differentiation could have resulted from genetic change or environmentally-driven phenotypic plasticity. Laboratory studies on A. sagrei from a population in Florida indicate that hindlimb length exhibits adaptive phenotypic plasticity. Further studies are required to determine if the observed differences among the experimental populations are the result of such plasticity. Regardless of whether the differences result from plasticity, genetic change, or both, the observation that anole populations differentiate rapidly and adaptively when exposed to novel environmental conditions has important implications for understanding the adaptive radiation of Caribbean anoles.     

Variation in scale numbers is consistent with ecologically based natural selection acting within and between lizard species

Recent studies have demonstrated that changes in scale number are correlated with ecological variables such as precipitation, and this suggests that scale number may be under selection to maintain water balance in reptiles. Here, we present new evidence that variation in scale numbers within and among species of Anolis lizards is under ecologically based natural selection. We measured scalation of the brown anole, Anolis sagrei, in two habitat types on each of five islands in the Bahamas. We also measured scalation for 12 species of anole representing six different ecomorphs from the Greater Antilles. Within populations of A. sagrei, scale numbers increased with increasing precipitation and with decreasing temperature in open arid habitats. Variation measured among species of Anolis from the Greater Antilles showed similar patterns with temperature, precipitation, and elevation. Independent contrasts using scale count data indicated that variation in scale number was congruent within and between species, even after accounting for the influence of phylogeny. We measured natural selection (survival to maturity) on scale number in A. sagrei over two different habitat types in the Bahamas. Patterns of natural selection were congruent with the correlational results described. Finally, results from a breeding experiment in the laboratory provide preliminary evidence that variation in scale number is heritable, and suggests a mechanism for generating these correlations. Our results provide new evidence that the diversification of anoles has been shaped by natural selection and that ecologically based selection pressures help explain diversification at both the population and species levels. Co-ordinating editor: M. Klaassen     

Establishment of <Emphasis Type="Italic">Anolis sagrei</Emphasis> on Bermuda represents a novel ecological threat to Critically Endangered Bermuda skinks (<Emphasis Type="Italic">Plestiodon longirostris</Emphasis>)

Bermuda is an isolated, oceanic island with only one endemic terrestrial vertebrate, the Critically Endangered Bermuda skink (Plestiodon longirostris; Squamata, Scincidae). Major declines in P. longirostris populations have been caused primarily by habitat loss and mortality via invasive species (e.g., predation from birds and cats) and human waste products (e.g., trapped in discarded bottles). However, biotic interactions and interspecific competition with invasive lizards have also been identified as potentially detrimental to P. longisrostris populations. Here, we provide the first occurrence records of a highly invasive lizard, the Cuban brown anole (Anolis sagrei), on Bermuda. We assess the brown anole’s diet, habitat use, morphology, and island-wide distribution for comparison to the native skink, P. longirostris. Results of this study indicate that A. sagrei in Bermuda are highly terrestrial (>60% of all lizards observed on the ground vs. in trees) and forage primarily on terrestrial invertebrates. These data indicate substantial ecological overlap with the exclusively-terrestrial P. longirostris. This is in contrast to the other established non-native lizards on Bermuda, which are principally arboreal and have successfully coexisted with P. longirostris for >60 years. At present, the geographic distributions of A. sagrei and P. longirostris do not overlap. However, all extant skink populations are within several kilometers of brown anole populations (with the nearest being <0.5 km). The extensive overlap in ecological niche between the Bermuda skink and the invasive brown anole will likely present a serious conservation threat if contact is made. This study is exceptional in providing clear in situ ecological data which predict a conservation threat of an established invasive species to a Critically Endangered island endemic prior to coexistence. Continued monitoring of this situation as P. longirostris and A. sagrei inevitably come into contact will allow these a priori hypotheses of conservation risk via ecological overlap to be tested.     

Spatial variation in climate mediates gene flow across an island archipelago

High levels of gene flow among partially isolated populations can overwhelm selection and limit local adaptation. This process, known as “gene swamping,” can homogenize genetic diversity among populations and reduce the capacity of a species to withstand rapid environmental change. We studied brown anole lizards (Anolis sagrei) distributed across seven islands in The Bahamas. We used microsatellite markers to estimate gene flow among islands and then examined the correlation between thermal performance and island temperature. The thermal optimum for sprint performance was correlated with both mean and maximum island temperature, whereas performance breadth was not correlated with any measure of temperature variation. Gene flow between islands decreased as the difference between mean island temperatures increased, even when those islands were adjacent to one another. These data suggest that phenotypic variation is the result of either (1) local genetic adaptation with selection against immigrants maintaining variation in the thermal optimum, (2) irreversible forms of adaptive plasticity such that immigrants have reduced fitness, or (3) an interaction between fixed genetic differences and plasticity. In general, the patterns of gene flow we observed suggest that local thermal environments represent important ecological filters that can mediate gene flow on relatively fine geographic scales.     

SEX‐SPECIFIC SELECTION AND INTRASPECIFIC VARIATION IN SEXUAL SIZE DIMORPHISM

Sexual size dimorphism (SSD) is thought to evolve due to sex differences in selection on body size, but it is largely unknown whether intraspecific variation in SSD reflects differences in sex‐specific selection among populations. We addressed this question by comparing viability selection between two island populations of the brown anole lizard (Anolis sagrei) that differ in the magnitude of male‐biased SSD. On both islands, females experienced stabilizing selection favoring intermediate size whereas males experienced directional selection favoring larger size. Thus, sex‐specific selection matched the overall pattern of male‐biased SSD, but population differences in the magnitude of SSD were not associated with local differences in selection. Rather, population differences in SSD appear to result from underlying differences in the environmental potential for a rapid growth, coupled with sex‐specific phenotypic plasticity. Males grew more slowly on the island with low SSD whereas growth of females did not differ between islands. Both sexes had substantially lower mass per unit length on the island with low SSD, suggesting that they were in a relatively poorer energetic condition. We propose that this energetic constraint disproportionately impacts growth of males due to their greater absolute energy requirements, thus driving intraspecific variation in SSD.     

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.     

Character displacement in the midst of background evolution in island populations of Anolis lizards: A spatiotemporal perspective

Negative interactions between species can generate divergent selection that causes character displacement. However, other processes cause similar divergence. We use spatial and temporal replication across island populations of Anolis lizards to assess the importance of negative interactions in driving trait shifts. Previous work showed that the establishment of Anolis sagrei on islands drove resident Anolis carolinensis to perch higher and evolve larger toepads. To further test the interaction's causality and predictability, we resurveyed a subset of islands nine years later. Anolis sagrei had established on one island between surveys. We found that A. carolinensis on this island now perch higher and have larger toepads. However, toepad morphology change on this island was not distinct from shifts on six other islands whose Anolis community composition had not changed. Thus, the presence of A. sagrei only partly explains A. carolinensis trait variation across space and time. We also found that A. carolinensis on islands with previously established A. sagrei now perch higher than a decade ago, and that current A. carolinensis perch height is correlated with A. sagrei density. Our results suggest that character displacement likely interacts with other evolutionary processes in this system, and that temporal data are key to detecting such interactions.     

Evidence for asymmetrical intraguild predation between native and introduced Anolis lizards

Since its introduction, Anolis sagrei (Sauria: Polychrotidae) has been replacing native A. carolinensis in Florida and native A. conspersus in Grand Cayman Island as the common anole of urban environments and other open habitats. To assess the likelihood that predation of juvenile native anoles by A. sagrei adults is an important interaction in this process, the propensities for intraguild predation and cannibalism were assessed for A. sagrei and A. carolinensis in Florida and for A. sagrei and A. conspersus in Grand Cayman. Predation experiments were conducted in cages, using freshly captured lizards, in which adult males of each species were presented with conspecific and heterospecific juveniles. Adult A. sagrei were (1) significantly more likely to eat juveniles than were adult A. carolinensis or A. conspersus, and (2) significantly more likely to eat heterospecific than conspecific juveniles, whereas adult A. carolinensis and A. conspersus were not. Thus, the propensity for intraguild predation is asymmetrical in favor of introduced A. sagrei in Florida and Grand Cayman. Further study is needed, however, to determine the importance of intraguild predation under field conditions. Received: 14 July 1999 / Accepted: 6 March 2000     

Habitat use and ecological interactions of an introduced and a native species of Anolis lizard on Grand Cayman,with a review of the outcomes of anole introductions

Since its introduction ten years ago, Anolis sagrei has spread over much of Grand Cayman and is now more common in some habitats than the native anole, A. conspersus. Interspecific differences in body size, perch height, and microclimatic preference may have facilitated the colonization. Nonetheless, competition may be occurring between the species; comparisons with studies of habitat use prior to the arrival of A. sagrei indicate that in open habitats, where A. sagrei is now abundant, A. conspersus perches higher, but in closed habitats, where A. sagrei is absent, no change in perch height is evident. Review of data concerning 23 Anolis introductions indicates that the presence or absence of an ecologically similar native species may be an important determinant of colonization success or failure.     

Parallel shifts in ecology and natural selection in an island lizard

Background  

Natural selection is a potent evolutionary force that shapes phenotypic variation to match ecological conditions. However, we know little about the year-to-year consistency of selection, or how inter-annual variation in ecology shapes adaptive landscapes and ultimately adaptive radiations. Here we combine remote sensing data, field experiments, and a four-year study of natural selection to show that changes in vegetation structure associated with a severe drought altered both habitat use and natural selection in the brown anole, Anolis sagrei.     

Pulses of marine subsidies amplify reproductive potential of lizards by increasing individual growth rate

Pulsed resource subsidies can have profound effects on recipient communities. The effects of resource pulses are often mediated by increases in the density of consumer populations. Here we investigate several mechanisms linking experimental pulses of seaweed deposition to population‐level responses in the brown anole Anolis sagrei. Subsidized lizards grew approximately 30% faster than lizards in seaweed‐removal plots, but there was no effect of seaweed subsidies on survival or body condition. Breeding is strongly seasonal in A. sagrei, resulting in a limited reproductive window of opportunity. Accelerated growth allows subsidized females to reach sexual maturity earlier and thereby exploit more of this window, which is projected to double fecundity in their first year of life. These results show how changes in an individual trait can translate pulses of resource input into reproductive output. Further, they highlight the importance of seasonal timing in mechanistically linking individual‐, population‐ and community‐level responses to pulsed resource subsidies.     

Isolation of polymorphic tetranucleotide microsatellite markers for the brown anole (Anolis sagrei)

Eleven polymorphic microsatellite markers have been developed for the brown anole, Anolis sagrei. The number of alleles range from five to 14 per locus with the observed heterozygosity ranging from 0.46 to 0.92. These markers will be useful for analysis of questions concerning population genetic structure and reproductive behaviour.     

Revealing the geographic origin of an invasive lizard: the problem of native population genetic diversity

The brown anole, Anolis sagrei, is one of the most widespread and successful colonisers of the diverse Anolis genus, which comprises c. 400 species occurring naturally in Central and South America and the Caribbean. Based on extensive between and within population sampling from a previously published study (334 mitochondrial DNA sequences) and sampling for this study (37 mtDNA sequences), we reconstruct a phylogeny and produce a haplotype network to assign a recently introduced population in St Vincent, Lesser Antilles to its geographic origin. A single haplotype was present in the St Vincent population, which was identical to a haplotype from Tampa, FL. We show that genetic diversity within native range populations, combined with low frequencies of introduced haplotypes in native ranges, may impair attempts to identify source populations, even despite intensive sampling effort. The absence of mtDNA haplotype diversity suggests a significant genetic founder effect within the St Vincent population.     

What determines dewlap diversity in Anolis lizards? An among‐island comparison

Animal signalling systems are extremely diverse as they are under different, often conflicting, selective pressures. A classic textbook example of a diverse signal is the anoline dewlap. Both at the inter‐ and intraspecific levels, dewlap size, colour, shape and pattern vary extensively. Here, we attempt to elucidate the various factors explaining the diversity in dewlap size and pattern among seven Anolis sagrei populations from different islands in the Bahamas. The seven islands differ in the surface area, number and kind of predators, sexual size dimorphism and Anolis species composition. In addition, we investigate whether selective pressures acting on dewlap design differ between males and females. Whereas dewlap pattern appears to serve a role in species recognition in both sexes, our data suggest that relative dewlap size is under natural and/or sexual selection. We find evidence for the role of the dewlap as a pursuit‐deterrence signal in both males and females as relative dewlap size is larger on islands where A. sagrei occurs sympatrically with predatory Leiocephalus lizards. Additionally, in males relatively large dewlaps seem to be selected for in a sexual context, whereas in females natural selection, for instance by other predators than Leiocephalus lizards, appears to constrain relative dewlap size.     

<Emphasis Type="Italic">Wolbachia</Emphasis>-induced cytoplasmic incompatibility in Japanese populations of <Emphasis Type="Italic">Tetranychus urticae</Emphasis> (Acari: Tetranychidae)

Intracellular bacteria of the genus Wolbachia (alpha Proteobacteria) induce cytoplasmic incompatibility (CI) in many arthropod species, including spider mites, but not all Wolbachia cause CI. In spider mites CI becomes apparent by a reduced egg hatchability and a lower daughter:son ratio: CI in haplodiploid organisms in general was expected to produce all-male offspring or a male-biased sex ratio without any death of eggs. In a previous study of Japanese populations of Tetranychus urticae, two out of three green-form populations tested were infected with non-CI Wolbachia strains, whereas none of six red-form populations harbored Wolbachia. As the survey of Wolbachia infection in T. urticae is still fragmentary in Japan, we checked Wolbachia infection in thirty green-form populations and 29 red-form populations collected from a wide range of Japanese islands. For Wolbachia-infected populations, we tested the effects of Wolbachia on the reproductive traits and determined the phylogenetic relationships of the different strains of Wolbachia. All but one green-form populations were infected with Wolbachia and all strains belonged to the subgroup Ori when the wsp gene was used to determine the phylogenetic relationships of different strains of Wolbachia. Six out of 29 red-form populations harbored Wolbachia and the infected strains belonged to the subgroups Ori and Bugs. Twenty-four of 29 infected green-form populations and five of six infected red-form populations induced CI among the hosts. Thus, CI-Wolbachia strains are widespread in Japan, and no geographical trend was observed in the CI-Wolbachia. Although three red-form populations harbored other intracellular bacteria Cardinium, they did not affect host reproduction.     

Species of Pleuroxus (Anomopoda,Chydoridae) from the subantarctic islands and southernmost South America: a partial unravelling of the Pleuroxus aduncus problem

Whereas previously all populations of Pleuroxus (now P.) known from the subantarctic islands and southernmost South America were considered to belong to a subspecies of P. aduncus (described from France), now there are five distinct species, only one of which resembles P. aduncus to any significant extent, but even it is a good species. Thus, the taxa are all distinctly different, and none of them could possibly be considered an infraspecies of P. aduncus sens. str. P. macquariensis from Macquarie Island and P. paroplesius and P. varidentatus from South America are new. Of the five species, P. varidentatus resembles P. aduncus most closely, but is separated from it by a number of significant characters. P. wittsteini is presently known from five islands in the south Indian Ocean, but there is considerable uncertainty as to whether all these populations really are the same taxon, because they differ somewhat in the shape of the labrum and in the intensity of sculpturing of the carapace and head. P. scopuliferus from South America is the most distinctive species of the group, having 9 gnathobasic filter setae on trunklimb III instead of the usual 8, a weak ridge on the shell, and a recurved rostrum extending beyond the tip of the labrum. No species of Pleuroxus (or of P., another subgenus of animals formerly assigned simply to Pleuroxus are known from the islands in the Scotia Arc between South America and Antarctica. The patterns of distribution cannot be explained by an on-going passive dispersal of resting eggs. No populations of species on the subantarctic islands are known from any of the southern land masses. Conditions on these islands intuitively must have been more severe during the glacial ages than during the present interglacial, suggesting that any anomopods present were eliminated during the severe glacial periods. Yet, the presence of isolated populations of endemic species on some islands and the complete lack of Pleuroxus on others (e.g. those in the Scotia Arc) argues that conditions, although more severe, still provided opportunities for the maintenance of active populations. Moreover, the morphological differences between populations of P. wittsteini on islands from a few hundred to several thousand kilometers apart likewise argue for genetic isolation over a very long period of time. Deceased     

Can rats prey on gull eggs? An experimental approach

Black rat Rattus rattus populations can reach high densities on the Mediterranean islands, as has been the case on the Chafarinas Islands (Western Mediterranean coast) in the last decade. This archipelago holds the second largest breeding population of Audouin's gull Larus audouinii and an important population of yellow-legged gull Larus cachinnans. Circumstantial evidences of rat predation upon Audouin's gull eggs led to conservation concerns about the impact of rat predation on gull productivity. We studied the impact of rats on gull nests experimentally by building artificial nests into the breeding area of yellow-legged gulls. Two kinds of eggs were placed in the artificial nests: manipulated eggs, in which the shell had been previously opened, and intact (unmanipulated) eggs. Rats preyed extensively on opened eggs but only once on intact eggs, apparently due to lack of skills to prey on intact eggs, suggesting that rats do not normally have access to fresh gull eggs. Rats inhabiting breeding areas of gulls can scavenge on broken eggs rolled out of the nest or on eggs with softened shells after nest desertion, but it is unlikely that they prey on natural gull nests guarded by parents. We suggest that introduced black rats on Mediterranean islands can only marginally affect the productivity of gulls owing to egg predation.     

Genetic variation in island populations of tuatara (<Emphasis Type="Italic">Sphenodon</Emphasis> spp) inferred from microsatellite markers

Tuatara (Sphenodon spp) populations are restricted to 35 offshore islands in the Hauraki Gulf, Bay of Plenty and Cook Strait of New Zealand. Low levels of genetic variation have previously been revealed by allozyme and mtDNA analyses. In this new study, we show that six polymorphic microsatellite loci display high levels of genetic variation in 14 populations across the geographic range of tuatara. These populations are characterised by disjunct allele frequency spectra with high numbers of private alleles. High F _ST (0.26) values indicate marked population structure and assignment tests allocate 96% of all individuals to their source populations. These genetic data confirm that islands support genetically distinct populations. Principal component analysis and allelic sequence data supplied information about genetic relationships between populations. Low numbers of rare alleles and low allelic richness identified populations with reduced genetic diversity. Little Barrier Island has very low numbers of old tuatara which have retained some relictual diversity. North Brother Island’s tuatara population is inbred with fixed alleles at 5 of the 6 loci.     

Communal egg-laying behaviour and the consequences of egg aggregation in the brown anole (Anolis sagrei)

Communal nesting is a behaviour that involves multiple females laying eggs in the same nest or nesting site. This behaviour may be a consequence of a shortage of preferable nest sites (constraint hypothesis) or an adaptation generated by fitness benefits associated with egg aggregation (adaptive hypothesis). Experimental tests of these hypotheses require information about maternal nest site choice and its fitness consequences. To address these, we studied a lizard (brown anole; Anolis sagrei) that produces single-egg clutches, but often aggregates eggs in nest sites. In a lab study, females were given the option of nesting in (a) soil previously used as nest substrate vs. fresh soil and (b) soil with eggshells vs. without eggshells. We also experimentally examined the effects of egg aggregation by incubating eggs singly, in groups of four, and in groups of nine. We recorded egg surface temperature, water uptake, and hatchling morphology. Females were more likely to nest in pots with used soil and with eggshells than in pots with fresh soil or without eggshells. We observed no effects of egg aggregation on egg survival, egg temperature, or most measures of hatchling morphology. However, singly-incubated eggs absorbed more water than eggs incubated in the four and nine egg aggregations and this resulted in offspring with greater body condition (i.e. heavier for their length) at hatching. The behavioural experiment demonstrates that females actively choose nest sites that have been used previously (as expected under the adaptive hypothesis), but the egg-aggregation experiment shows no benefits to offspring based on the variables measured. Thus, results of the behaviour study support the adaptive hypothesis; however, results from our egg-incubation study do not. Likely, the adaptive and constraint hypotheses are not mutually exclusive, and a diversity of factors influence the evolution of communal nesting behaviour.     

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.