Signals of differential introgression in the genome of natural hybrids of Caribbean anoles.

Hybridization facilitates recombination between divergent genetic lineages and can be shaped by both neutral and selective processes. Upon hybridization, loci with no net fitness effects introgress randomly from parental species into the genomes of hybrid individuals. Conversely, alleles from one parental species at some loci may provide a selective advantage to hybrids, resulting in patterns of introgression that do not conform to random expectations. We investigated genomic patterns of differential introgression in natural hybrids of two species of Caribbean anoles, Anolis pulchellus and A. krugi in Puerto Rico. Hybrids exhibit A. pulchellus phenotypes but possess A. krugi mitochondrial DNA, originated from multiple, independent hybridization events, and appear to have replaced pure A. pulchellus across a large area in western Puerto Rico. Combining genome-wide SNP datasets with bioinformatic methods to identify signals of differential introgression in hybrids, we demonstrate that the genomes of hybrids are dominated by pulchellus-derived alleles and show only 10%-20% A. krugi ancestry. The majority of A. krugi loci in hybrids exhibit a signal of non-random differential introgression and include loci linked to genes involved in development and immune function. Three of these genes (delta like canonical notch ligand 1, jagged1 and notch receptor 1) affect cell differentiation and growth and interact with mitochondrial function. Our results suggest that differential non-random introgression for a subset of loci may be driven by selection favouring the inheritance of compatible mitochondrial and nuclear-encoded genes in hybrids.

A biographical account of John Paul Richard Thomas, the man who leaves no stone unturned.

This biographical account summarizes the professional career and scientific contributions of John Paul Richard Thomas, a contemporary leading figure in the systematics of West Indian amphibians and non-avian reptiles, especially of blind snakes of the families Typhlopidae and Leptotyphlopidae. Since his first expedition to the West Indies in 1957, Richard's vast field experience (including three trips to Peru between 1968 and 1974), impressive collecting skills, and remarkable ability to detect phenotypic variation among natural populations have resulted in the description of more than 70 species of snakes (24 typhlopids, 4 leptotyphlopids), lizards, and frogs in 16 genera and 11 taxonomic families. Richard joined the faculty of the Department of Biology, University of Puerto Rico, Río Piedras, in 1976 and ever since his efforts significantly advanced organismal biology research at the institution. Although primarily a systematist, his desire to understand multiple aspects of an organism's biology and contagious passion for becoming intimately familiar with animals in their natural environments provided his students the opportunity to conduct research in fields such as behavioral and evolutionary ecology. Richard's mentoring fostered the scientific interests of his graduate students, who were exposed first-hand to every aspect of research, an invaluable experience that served as a springboard for the development of their professional careers inside and outside academia. This Commentary is a fitting tribute to an influential, unassuming scientist whose passion for turning over rocks has led to the discovery of many interesting species.

ORIGINS AND GENETIC DIVERSITY OF INTRODUCED POPULATIONS OF THE PUERTO RICAN RED-EYED COQUÍ, ELEUTHERODACTYLUS ANTILLENSIS, IN SAINT CROIX (U.S. VIRGIN ISLANDS) AND PANAMÁ.

The Red-eyed Coquí, Eleutherodactylus antillensis, is a terrestrial frog endemic to the Puerto Rican Bank (Puerto Rico and numerous islands and cays off its eastern coast), in the eastern Caribbean Sea. The species was likely introduced in Saint Croix, an island c. 100 km southeast of Puerto Rico, in the late 1930s, and in Panamá City, Panamá, in the late 1950s or early 1960s, but the source(s) of these introductions are unknown. We analyzed sequence data from one mtDNA locus and four nuDNA introns to infer the origin(s) of the Saint Croix and Panamá City populations and quantify their genetic diversity. Saint Croix and Panamanian populations do not share any haplotypes, and they cluster with different native populations, suggesting that they are derived from separate sources in the Puerto Rican Bank. Patterns of population structure trace the probable sources of E. antillensis in Saint Croix to islands off Puerto Rico's eastern coast, which include Vieques, Culebra, Saint Thomas, Saint John, Tortola, and Virgin Gorda, and possibly to eastern Puerto Rico as well. In contrast, Panamá City E. antillensis probably originated from either western or eastern Puerto Rico. Genetic diversity in the introduced populations is similar to or lower than in populations in the species' native range, indicating that genetic diversity has not increased in the alien frogs. Our findings may facilitate the development of preventive measures to minimize introductions of non-native amphibians in the Caribbean and Central America.

Climate as a driver of tropical insular diversity: comparative phylogeography of two ecologically distinctive frogs in Puerto Rico.

The effects of late Quaternary climate on distributions and evolutionary dynamics of insular species are poorly understood in most tropical archipelagoes. We used ecological niche models under past and current climate to derive hypotheses regarding how stable climatic conditions shaped genetic diversity in two ecologically distinctive frogs in Puerto Rico. Whereas the Mountain Coquí, Eleutherodactylus portoricensis, is restricted to montane forest in the Cayey and Luquillo Mountains, the Red-eyed Coquí, E. antillensis, is a habitat generalist distributed across the entire Puerto Rican Bank (Puerto Rico and the Virgin Islands, excluding St. Croix). To test our hypotheses, we conducted phylogeographic and population genetic analyses based on mitochondrial and nuclear loci of each species across their range in Puerto Rico. Patterns of population differentiation in E. portoricensis, but not in E. antillensis, supported our hypotheses. For E. portoricensis, these patterns include: individuals isolated by long-term unsuitable climate in the Río Grande de Loíza Basin in eastern Puerto Rico belong to different genetic clusters; past and current climate strongly predicted genetic differentiation; and Cayey and Luquillo Mountains populations split prior to the last interglacial. For E. antillensis, these patterns include: genetic clusters did not fully correspond to predicted long-term unsuitable climate; and past and current climate weakly predicted patterns of genetic differentiation. Genetic signatures in E. antillensis are consistent with a recent range expansion into western Puerto Rico, possibly resulting from climate change and anthropogenic influences. As predicted, regions with a large area of long-term suitable climate were associated with higher genetic diversity in both species, suggesting larger and more stable populations. Finally, we discussed the implications of our findings for developing evidence-based management decisions for E. portoricensis, a taxon of special concern. Our findings illustrate the role of persistent suitable climatic conditions in promoting the persistence and diversification of tropical island organisms.

Genetic divergence and diversity in the Mona and Virgin Islands Boas, Chilabothrus monensis (Epicrates monensis) (Serpentes: Boidae), West Indian snakes of special conservation concern.

Habitat fragmentation reduces the extent and connectivity of suitable habitats, and can lead to changes in population genetic structure. Limited gene flow among isolated demes can result in increased genetic divergence among populations, and decreased genetic diversity within demes. We assessed patterns of genetic variation in the Caribbean boa Chilabothrus monensis (Epicrates monensis) using two mitochondrial and seven nuclear markers, and relying on the largest number of specimens of these snakes examined to date. Two disjunct subspecies of C. monensis are recognized: the threatened C. m. monensis, endemic to Mona Island, and the rare and endangered C. m. granti, which occurs on various islands of the Puerto Rican Bank. Mitochondrial and nuclear markers revealed unambiguous genetic differences between the taxa, and coalescent species delimitation methods indicated that these snakes likely are different evolutionary lineages, which we recognize at the species level, C. monensis and C. granti. All examined loci in C. monensis (sensu stricto) are monomorphic, which may indicate a recent bottleneck event. Each population of C. granti exclusively contains private mtDNA haplotypes, but five of the seven nuclear genes assayed are monomorphic, and nucleotide diversity is low in the two remaining markers. The faster pace of evolution of mtDNA possibly reflects the present-day isolation of populations of C. granti, whereas the slower substitution rate of nuDNA may instead mirror the relatively recent episodes of connectivity among the populations facilitated by the lower sea level during the Pleistocene. The small degree of overall genetic variation in C. granti suggests that demes of this snake could be managed as a single unit, a practice that would significantly increase their effective population size.

Reproductive tradeoff limits the predatory efficiency of female Arizona Bark Scorpions (Centruroides sculpturatus).

BACKGROUND: Life history tradeoffs may result from temporal and physiological constraints intrinsic to an organism. When faced with limited time and energy, compromises occur and these resources are allocated among essential activities, such as body growth, maintenance, foraging, mating, and offspring care. We investigated potential tradeoffs that may occur between reproductive activities and feeding performance in female Arizona Bark Scorpions (Centruroides sculpturatus) by comparing the time taken to capture prey between non-reproductive and reproductive females (gravid females and females exhibiting maternal care, i.e. carrying offspring on their backs). RESULTS: Gravid females were as efficient at catching prey as non-gravid females. To control for variation in the duration of the maternal care period, we removed all offspring from all post-parturient females after 5 days. Brooding females and females 24 hours following offspring removal (FOR) did not successfully capture prey within the 900-second trial period. Twenty-eight days FOR, females caught prey faster than females displaying maternal care and females 24 hours FOR, but were not as efficient at catching prey as non-gravid and gravid females. When pursuing prey, C. sculpturatus exhibiting maternal care used an active foraging strategy more frequently than non-gravid, gravid, and females 28 days FOR. In contrast, non-gravid, gravid, and females 28 days FOR used active and ambush foraging with similar frequency. CONCLUSIONS: Our data suggest that reproduction does not significantly reduce the predatory efficiency of gravid C. sculpturatus, and that these females can cope with increasing body mass and the physiological costs of gestation. However, the observation that brooding females and females 24 hours FOR did not catch prey within the trial period indicates that maternal care significantly reduces predatory efficiency in these scorpions. Females 28 days FOR were still not as efficient at catching prey as non-gravid and gravid females, suggesting that reproductive costs extend for at least 4 weeks after the end of the maternal care period. Preferential use of an active foraging strategy by brooding females may increase prey encounter rates, allowing the scorpions to more rapidly replenish energy reserves depleted during reproduction. However, active foraging may be energetically costly and increase predation risk for brooding females. Our findings regarding antagonistic interactions between reproduction and feeding in female C. sculpturatus demonstrate the pervasive nature of reproductive costs for viviparous females, and may provide insight on factors that influence the diversity of reproductive strategies observed in nature.

Sea level, topography and island diversity: phylogeography of the Puerto Rican Red-eyed Coquí, Eleutherodactylus antillensis.

Quaternary climatic oscillations caused changes in sea level that altered the size, number and degree of isolation of islands, particularly in land-bridge archipelagoes. Elucidating the demographic effects of these oscillations increases our understanding of the role of climate change in shaping evolutionary processes in archipelagoes. The Puerto Rican Bank (PRB) (Puerto Rico and the Eastern Islands, which comprise Vieques, Culebra, the Virgin Islands and associated islets) in the eastern Caribbean Sea periodically coalesced during glaciations and fragmented during interglacial periods of the quaternary. To explore population-level consequences of sea level changes, we studied the phylogeography of the frog Eleutherodactylus antillensis across the archipelago. We tested hypotheses encompassing vicariance and dispersal narratives by sequencing mtDNA (c. 552 bp) of 285 individuals from 58 localities, and four nuDNA introns (totalling c. 1633 bp) from 173 of these individuals. We found low support for a hypothesis of divergence of the Eastern Islands populations prior to the start of the penultimate interglacial c. 250 kya, and higher support for a hypothesis of colonization of the Eastern Islands from sources in eastern Puerto Rico during the penultimate and last glacial period, when a land bridge united the PRB. The Río Grande de Loíza Basin in eastern Puerto Rico delineates a phylogeographic break. Haplotypes shared between the PRB and St. Croix (an island c. 105 km south-east of this archipelago) likely represent human-mediated introductions. Our findings illustrate how varying degrees of connectivity and isolation influence the evolution of tropical island organisms.

Climatic stability and genetic divergence in the tropical insular lizard Anolis krugi, the Puerto Rican 'Lagartijo Jardinero de la Montaña'.

Two factors that can lead to geographic structuring in conspecific populations are barriers to dispersal and climatic stability. Populations that occur in different physiographic regions may be restricted to those areas by physical and/or ecological barriers, which may facilitate the formation of phylogeographic clades. Long-term climatic stability can also promote genetic diversification, because new clades are more likely to evolve in areas that experience lesser climatic shifts. We conducted a phylogeographic study of the Puerto Rican lizard Anolis krugi to assess whether populations of this anole show genetic discontinuities across the species' range, and if they do, whether these breaks coincide with the boundaries of the five physiographic regions of Puerto Rico. We also assessed whether interpopulation genetic distances in A. krugi are positively correlated with relative climatic stability in the island. Anolis krugi exhibits genetic structuring, but the phylogroups do not correspond to the physiographic regions of Puerto Rico. We used climatic reconstructions of two environmental extremes of the Quaternary period, the present conditions and those during the last glacial maximum (LGM), to quantify the degree of climatic stability between sampling locations. We documented positive correlations between genetic distances and relative climatic stability, although these associations were not significant when corrected for autocorrelation. Principal component analyses indicated the existence of climatic niche differences between some phylogeographic clades of A. krugi. The approach that we employed to assess the relationship between climatic stability and the genetic architecture of A. krugi can also be used to investigate the impact of factors such as the spatial distribution of food sources, parasites, predators or competitors on the genetic landscape of a species.

Genetic structuring in the threatened "Lagartijo del Bosque Seco" (Anolis cooki) from Puerto Rico.

Species with restricted geographic distributions consisting of isolated populations are particularly susceptible to extinction because these demes face an increased risk of disappearing due to environmental, demographic, and genetic stochasticity. We used partial DNA sequences of the cytochrome b (1083 bp) and ND2 (1041 bp) mitochondrial genes to investigate the phylogeography and population genetics of Anolis cooki, a threatened lizard endemic to the southwestern coast of the Caribbean Island of Puerto Rico. Maximum likelihood and Bayesian methods revealed relatively shallow genetic differentiation among 27 unique haplotypes (from 52 individuals) from the known extant populations of A. cooki in mainland Puerto Rico. Despite this pattern, specimens from the same geographic area tended to nest together. The most basal division within A. cooki is between haplotypes from the three westernmost populations (Punta Aguila, Morrillos, Playa Santa) and the remainder demes (Bahía Ballena, La Cueva, Punta Verraco). The three westernmost populations of A. cooki are separated from their conspecific demes by the Guánica Bay and the Loco River drainage system, which together may represent a physiographic barrier for A. cooki. Each population of A. cooki only has private haplotypes; in other words, there are no shared mitochondrial types between populations. Because the number of private haplotypes can be used as an indirect measure of gene flow, this finding suggests that currently there is no migration among demes, and that each is an independent demographic unit, despite the relatively short distances (ca. 2 km) that separate some of them. Pairwise F(ST) values and spatial analyses of molecular variation confirmed the existence of distinct groups of genetically defined sampling areas, and of significant molecular variation among populations within groups and within populations. The conservation status of the populations of A. cooki varies greatly. The demes from Punta Aguila, Morrillos, and Bahía Ballena inhabit protected areas, and are larger, genetically diverse, and seemingly stable. The population from Playa Santa showed a high level of genetic diversity, but it occurs in an area that has been intensively developed for residential and touristic purposes, and its long-term survival is uncertain. A. cooki is also known from Caja de Muertos, an island off the southcentral coast of Puerto Rico. Surveys conducted on September 2006 and March 2007 did not produce any specimens, and a thorough assessment of Caja de Muertos is needed to determine the present status of A. cooki on the island.

Historical contingency and animal diets: the origins of egg eating in snakes.

Evolutionary changes in animal diets must often begin through the inclusion of a novel food type as a minor component of the diet. An aspect of this initial change that has rarely been studied is the relationship between the existing diet and the use of specific novel foods. We used comparative analyses to test the hypothesis that, in snakes, feeding on squamate (lizard and snake) eggs or bird eggs--items that represent evolutionarily derived and, in most cases, minor components of the diet--is associated with feeding on squamates or birds, respectively. Phylogenetic concentrated-changes tests indicate a significant tendency for predation on eggs to arise in snake lineages characterized by feeding on the corresponding animals. These results also generally hold for analyses including only snake species that are likely to encounter eggs and are large enough to ingest them. The inferred histories of specialized egg eaters also support the hypothesis. Because snakes often use chemical cues to recognize prey, the observed phylogenetic patterns might be explained by chemical similarities between eggs and adult animals. Our results suggest broad effects of predispositions on snake diets and thus illustrate how historical contingencies can shape the ecology of organisms.

An experimental study of interspecific interactions between two Puerto Rican Anolis lizards.

We analyzed the impact of interspecific interactions between two ecologically and morphologically distinct Puerto Rican lizards, Anolis gundlachi and A. evermanni, in an experimental design consisting of six 20 × 20 m plots divided into three blocks, each consisting of a pair of experimental and control plots. We removed A. gundlachi from experimental plots and monitored the response of A. evermanni. The reduction in the number of A. gundlachi resulted in a significant increase in the abundance of both adult and juvenile A. evermanni. We found no evidence for a shift in structural habitat use in A. evermanni in experimental plots. Two possible mechanisms, interspecific competition and intraguild predation, could explain the increase in abundance of A. evermanni after the removal of A. gundlachi. These results make clear that interactions still occur between A. gundlachi and A. evermanni even given their morphological and ecological differences.