Jason J. Kolbe

Genetic variation increases during biological invasion by a Cuban lizard

A genetic paradox exists in invasion biology: how do introduced populations, whose genetic variation has probably been depleted by population bottlenecks, persist and adapt to new conditions? Lessons from conservation genetics show that reduced genetic variation due to genetic drift and founder effects limits the ability of a population to adapt, and small population size increases the risk of extinction. Nonetheless, many introduced species experiencing these same conditions during initial introductions persist, expand their ranges, evolve rapidly and become invasive. To address this issue, we studied the brown anole, a worldwide invasive lizard. Genetic analyses indicate that at least eight introductions have occurred in Florida from across this lizards native range, blending genetic variation from different geographic source populations and producing populations that contain substantially more, not less, genetic variation than native populations. Moreover, recently introduced brown anole populations around the world originate from Florida, and some have maintained these elevated levels of genetic variation. Here we show that one key to invasion success may be the occurrence of multiple introductions that transform among-population variation in native ranges to within-population variation in introduced areas. Furthermore, these genetically variable populations may be particularly potent sources for introductions elsewhere. The growing problem of invasive species introductions brings considerable economic and biological costs. If these costs are to be mitigated, a greater understanding of the causes, progression and consequences of biological invasions is needed.

IMPACT OF NEST-SITE SELECTION ON NEST SUCCESS AND NEST TEMPERATURE IN NATURAL AND DISTURBED HABITATS

Nest-site selection behavior is a maternal effect that contributes to offspring survival and variation in offspring phenotypes that are subject to natural selection. We investigated nest-site selection and its consequences in the snapping turtle, Chelydra ser- pentina, in northwestern Illinois. We evaluated nest-site selection at both the microhabitat and habitat patch levels. Turtles selected nest sites with shorter vegetation, more open sand, and fewer cacti than random locations. These microhabitat characteristics described sandy patches where both nest density and success were higher compared to grassy patches in 1999. We subsequently investigated nest-site selection within two discrete subdivisions of the study area that varied in the degree of human disturbance to determine if nesting behavior, nest success, or nest temperatures were affected. The tendency to nest in sandy patches was much stronger at the natural site due to habitat modifications at the residential site that have blurred the distinction between sandy and grassy patches. Additionally, the residential site had a high density of nests within 5 m of houses and a fence (both areas with disturbed habitat similar to sandy patches), compared to the overall density. Thus, nest success associated with sandy patches may be compromised at the residential site; an ecological trap may result in lower nest success in areas with preferred microhabitat char- acteristics. Despite a similar basis for nest-site selection in terms of microhabitat charac- teristics at both sites, nest temperatures were correlated with microhabitat characteristics used to select nest sites only at the natural site. Nest temperatures at the residential site were instead correlated only with the percentage overstory vegetation cover and therefore averaged 2 8C lower than at the natural site, a temperature difference that influenced offspring sex. The higher percentage overstory vegetation cover at the residential site was due to human alterations of the habitat, and may serve to extend the ecological trap biasing the sex ratio of this population. This study illustrates the importance of (1) nest-site selection as a substantive maternal effect, (2) understanding habitat use during crucial life-history events, and (3) the potential for human disturbance to modify offspring phenotypes and negatively impact nest success despite adaptive nesting behavior.

CONVERGENCE AND THE MULTIDIMENSIONAL NICHE

Abstract Convergent evolution has played an important role in the development of the ecological niche concept. We investigated patterns of convergent and divergent evolution of Caribbean Anolis lizards. These lizards diversified independently on each of the islands of the Greater Antilles, producing the same set of habitat specialists on each island. Using a phylogenetic comparative framework, we examined patterns of morphological convergence in five functionally distinct sets of morphological characters: body size, body shape, head shape, lamella number, and sexual size dimorphism. We find evidence for convergence among members of the habitat specialist types for each of these five datasets. Furthermore, the patterns of convergence differ among at least four of the five datasets; habitat specialists that are similar for one set of characters are often greatly different for another. This suggests that the habitat specialist niches into which these anoles have evolved are multidimensional, involving several distinct and independent aspects of morphology.

Admixture determines genetic diversity and population differentiation in the biological invasion of a lizard species

Molecular genetic analyses show that introduced populations undergoing biological invasions often bring together individuals from genetically disparate native-range source populations, which can elevate genotypic variation if these individuals interbreed. Differential admixture among multiple native-range sources explains mitochondrial haplotypic diversity within and differentiation among invasive populations of the lizard Anolis sagrei. Our examination of microsatellite variation supports the hypothesis that lizards from disparate native-range sources, identified using mtDNA haplotypes, form genetically admixed introduced populations. Furthermore, within-population genotypic diversity increases with the number of sources and among-population genotypic differentiation reflects disparity in their native-range sources. If adaptive genetic variation is similarly restructured, then the ability of invasive species to adapt to new conditions may be enhanced.

A PHYLOGENETIC TEST FOR ADAPTIVE CONVERGENCE IN ROCK-DWELLING LIZARDS

Abstract Phenotypic similarity of species occupying similar habitats has long been taken as strong evidence of adaptation, but this approach implicitly assumes that similarity is evolutionarily derived. However, even derived similarities may not represent convergent adaptation if the similarities did not evolve as a result of the same selection pressures; an alternative possibility is that the similar features evolved for different reasons, but subsequently allowed the species to occupy the same habitat, in which case the convergent evolution of the same feature by species occupying similar habitats would be the result of exaptation. Many lizard lineages have evolved to occupy vertical rock surfaces, a habitat that places strong functional and ecological demands on lizards. We examined four clades in which species that use vertical rock surfaces exhibit long hindlimbs and flattened bodies. Morphological change on the phylogenetic branches leading to the rock-dwelling species in the four clades differed from change on other branches of the phylogeny; evolutionary transitions to rock-dwelling generally were associated with increases in limb length and decreases in head depth. Examination of particular characters revealed several different patterns of evolutionary change. Rock-dwelling lizards exhibited similarities in head depth as a result of both adaptation and exaptation. Moreover, even though rock-dwelling species generally had longer limbs than their close relatives, clade-level differences in limb length led to an overall lack of difference between rock- and non-rock-dwelling lizards. These results indicate that evolutionary change in the same direction in independent lineages does not necessarily produce convergence, and that the existence of similar advantageous structures among species independently occupying the same environment may not indicate adaptation.

PHYLOGENETIC ANALYSIS OF ECOLOGICAL AND MORPHOLOGICAL DIVERSIFICATION IN HISPANIOLAN TRUNK-GROUND ANOLES (ANOLIS CYBOTES GROUP)

Abstract Anolis lizards in the Greater Antilles partition the structural microhabitats available at a given site into four to six distinct categories. Most microhabitat specialists, or ecomorphs, have evolved only once on each island, yet closely related species of the same ecomorph occur in different geographic macrohabitats across the island. The extent to which closely related species of the same ecomorph have diverged to adapt to different geographic macro‐habitats is largely undocumented. On the island of Hispaniola, members of the Anolis cybotes species group belong to the trunk‐ground ecomorph category. Despite evolutionary stability of their trunk‐ground microhabitat, populations of the A. cybotes group have undergone an evolutionary radiation associated with geographically distinct macrohabitats. A combined phylogeographic and morphometric study of this group reveals a strong association between macrohabitat type and morphology independent of phylogeny. This association results from long‐term morphological evolutionary stasis in populations associated with mesic‐forest environments (A. c. cybotes and A. marcanoi) and predictable morphometric changes associated with entry into new macrohabitat types (i.e., xeric forests, high‐altitude pine forest, rock outcrops). Phylogeographic analysis of 73 new mitochondrial DNA sequences (1921 aligned sites) sampled from 68 geographic populations representing 12 recognized species and subspecies diagnoses 16 allopatric or parapatric groupings of populations differing from each other by 5–18% sequence divergence. At least some of these groupings appear to have attained species‐level divergence from others. Evolutionary specialization to different macrohabitat types may be a major factor in the evolutionary diversification of Greater Antillean anoles.

Differential admixture shapes morphological variation among invasive populations of the lizard Anolis sagrei.

The biological invasion of the lizard Anolis sagrei provides an opportunity to study evolutionary mechanisms that produce morphological differentiation among non‐native populations. Because the A. sagrei invasion represents multiple native‐range source populations, differential admixture as well as random genetic drift and natural selection, could shape morphological evolution during the invasion. Mitochondrial DNA (mtDNA) analyses reveal seven distinct native‐range source populations for 10 introduced A. sagrei populations from Florida, Louisiana and Texas (USA), and Grand Cayman, with 2–5 native‐range sources contributing to each non‐native population. These introduced populations differ significantly in frequencies of haplotypes from different native‐range sources and in body size, toepad‐lamella number, and body shape. Variation among introduced populations for both lamella number and body shape is explained by differential admixture of various source populations; mean morphological values of introduced populations are correlated with the relative genetic contributions from different native‐range source populations. The number of source populations contributing to an introduced population correlates with body size, which appears independent of the relative contributions of particular source populations. Thus, differential admixture of various native‐range source populations explains morphological differences among introduced A. sagrei populations. Morphological differentiation among populations is compatible with the hypothesis of selective neutrality, although we are unable to test the hypothesis of interdemic selection among introductions from different native‐range source populations.

Founder Effects Persist Despite Adaptive Differentiation: A Field Experiment with Lizards

Random and Directed Natural selection drives populations to adapt to new environments; the raw material or “founder effects” provided by the first colonizing individuals can thus have a formative influence on the populations future. Kolbe et al. (p. 1086, published online 2 February; see the cover) tested the relative contributions of selection and founder effects in Bahamian lizards. Founders were taken from an island covered in forest: These lizards had long hindlimbs for sprinting across the broad expanses of tree trunks. Long-limbed lizards were introduced to seven smaller islands covered in scrub that, before hurricane Frances in 2004 swept them away, had been populated by lizards with short hindlimbs better suited for navigating a twiggy habitat. After several generations, all the new lizard populations had adapted to their new habitats by evolving shorter hindlimbs but they also retained other morphological and genetic signatures from their founding ancestors. Thus, evolution occurs by a combination of arbitrary events, as well as those shaped by selection. Introduced populations of anoles retain characteristics of their founders and acquire adaptations to their new environment. The extent to which random processes such as founder events contribute to evolutionary divergence is a long-standing controversy in evolutionary biology. To determine the respective contributions of founder effects and natural selection, we conducted an experiment in which brown anole (Anolis sagrei) lizard populations were established on seven small islands in the Bahamas, from male-female pairs randomly drawn from the same large-island source. These founding events generated significant among-island genetic and morphological differences that persisted throughout the course of the experiment despite all populations adapting in the predicted direction—shorter hindlimbs—in response to the narrower vegetation on the small islands. Thus, using a replicated experiment in nature, we showed that both founder effects and natural selection jointly determine trait values in these populations.

Adaptation, Speciation, and Convergence: A Hierarchical Analysis of Adaptive Radiation in Caribbean Anolis Lizards

Abstract Caribbean Anolis lizards are a classic case of adaptive radiation, repeated four times across islands of the Greater Antilles. On each island, very similar patterns of evolutionary divergence have occurred, resulting in the evolution of the same set of ecological specialists—termed ecomorphs—on each island. However, this is only part of the story of the Caribbean anole radiations. Indeed, much of the species diversity of Caribbean Anolis occurs within clades of ecomorphs, which contain as many as 14 ecologically-similar species on a single island. We ask to what extent the classic model of ecological interactions as the driving force in adaptive radiation can account for this aspect of anole evolutionary diversity. Our answer is that it can in part, but not entirely. More generally, the most complete understanding of evolutionary diversification and radiation is achieved by studying multiple hierarchical evolutionary levels from clades to populations.

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.