Kyle Summers

Interspecific and intraspecific views of color signals in the strawberry poison frog Dendrobates pumilio.

SUMMARY Poison frogs in the anuran family Dendrobatidae use bright colors on their bodies to advertise toxicity. The species Dendrobates pumilio Schmidt 1858, the strawberry poison frog, shows extreme polymorphism in color and pattern in Panama. It is known that females of D. pumilio preferentially choose mates of their own color morph. Nevertheless, potential predators must clearly see and recognize all color morphs if the aposematic signaling system is to function effectively. We examined the ability of conspecifics and a model predator to discriminate a diverse selection of D. pumilio colors from each other and from background colors. Microspectrophotometry of isolated rod and cone photoreceptors of D. pumilio revealed the presence of a trichromatic photopic visual system. A typical tetrachromatic bird system was used for the model predator. Reflectance spectra of frog and background colors were obtained, and discrimination among spectra in natural illuminants was mathematically modeled. The results revealed that both D. pumilio and the model predator discriminate most colors quite well, both from each other and from typical backgrounds, with the predator generally performing somewhat better than the conspecifics. Each color morph displayed at least one color signal that is highly visible against backgrounds to both visual systems. Our results indicate that the colors displayed by the various color morphs of D. pumilio are effective signals both to conspecifics and to a model predator.

Amazonian Amphibian Diversity Is Primarily Derived from Late Miocene Andean Lineages

The Neotropics contains half of remaining rainforests and Earths largest reservoir of amphibian biodiversity. However, determinants of Neotropical biodiversity (i.e., vicariance, dispersals, extinctions, and radiations) earlier than the Quaternary are largely unstudied. Using a novel method of ancestral area reconstruction and relaxed Bayesian clock analyses, we reconstructed the biogeography of the poison frog clade (Dendrobatidae). We rejected an Amazonian center-of-origin in favor of a complex connectivity model expanding over the Neotropics. We inferred 14 dispersals into and 18 out of Amazonia to adjacent regions; the Andes were the major source of dispersals into Amazonia. We found three episodes of lineage dispersal with two interleaved periods of vicariant events between South and Central America. During the late Miocene, Amazonian, and Central American-Chocoan lineages significantly increased their diversity compared to the Andean and Guianan-Venezuelan-Brazilian Shield counterparts. Significant percentage of dendrobatid diversity in Amazonia and Chocó resulted from repeated immigrations, with radiations at <10.0 million years ago (MYA), rather than in situ diversification. In contrast, the Andes, Venezuelan Highlands, and Guiana Shield have undergone extended in situ diversification at near constant rate since the Oligocene. The effects of Miocene paleogeographic events on Neotropical diversification dynamics provided the framework under which Quaternary patterns of endemism evolved.

Visual mate choice in poison frogs.

We investigated female mate choice on the basis of visual cues in two populations of Dendrobates pumilio, the strawberry poison frog, from the Bocas del Toro Archipelago in Panama, Central America. Mate choice experiments were carried out by presenting subject females of each of two morphs of this species (orange and green) from two different island populations (Nancy Key and Pope Island) with object frogs (one of each morph) under glass at one end of a terrarium. Recorded calls were played simultaneously from behind both object frogs. The experiments were carried out under two light regimes: (i) white light, and (ii) relatively monochromatic filtered blue light. Subject females from each population displayed a significant preference for their own morph under white light, but not under blue light. These results indicate that female D. pumilio use visual cues in mate choice, and suggest that colour may be the visual cue they use.

The evolution of coloration and toxicity in the poison frog family (Dendrobatidae)

The poison frogs (family Dendrobatidae) are terrestrial anuran amphibians displaying a wide range of coloration and toxicity. These frogs generally have been considered to be aposematic, but relatively little research has been carried out to test the predictions of this hypothesis. Here we use a comparative approach to test one prediction of the hypothesis of aposematism: that coloration will evolve in tandem with toxicity. Recently, we developed a phylogenetic hypothesis of the evolutionary relationships among representative species of poison frogs, using sequences from three regions of mitochondrial DNA. In our analysis, we use that DNA-based phylogeny and comparative analysis of independent contrasts to investigate the correlation between coloration and toxicity in the poison frog family (Dendrobatidae). Information on the toxicity of different species was obtained from the literature. Two different measures of the brightness and extent of coloration were used. (i) Twenty-four human observers were asked to rank different photos of each different species in the analysis in terms of contrast to a leaf-littered background. (ii) Color photos of each species were scanned into a computer and a computer program was used to obtain a measure of the contrast of the colors of each species relative to a leaf-littered background. Comparative analyses of the results were carried out with two different models of character evolution: gradual change, with branch lengths proportional to the amount of genetic change, and punctuational change, with all change being associated with speciation events. Comparative analysis using either method or model indicated a significant correlation between the evolution of toxicity and coloration across this family. These results are consistent with the hypothesis that coloration in this group is aposematic.

Genetic structure is correlated with phenotypic divergence rather than geographic isolation in the highly polymorphic strawberry poison‐dart frog

Phenotypic and genetic divergence can be influenced by a variety of factors, including sexual and natural selection, genetic drift and geographic isolation. Investigating the roles of these factors in natural systems can provide insight into the relative influences of allopatric and ecological modes of biological diversification in nature. The strawberry poison frog, Dendrobates pumilio, presents an excellent opportunity for this kind of research, displaying a diverse array of colour morphs and inhabiting a heterogeneous landscape that includes oceanic islands, fragmented rainforest patches and wide expanses of suitable habitat. In this study, we use 15 highly polymorphic microsatellite loci to estimate population structure and gene flow among populations from across the range of D. pumilio and a causal modelling framework to statistically test 12 hypotheses regarding the geographic and phenotypic variables that explain genetic differentiation within this system. Our results demonstrate that the genetic distance between populations is most strongly associated with differences in dorsal coloration. Previous experimental studies have shown that phenotypic differences can result in sexual and natural selection against non‐native phenotypes, and our results now show that these forces lead to genetic isolation between different colour morphs in the wild, presenting a potential case of incipient speciation through selection.

Adaptive evolution of genes underlying schizophrenia

Schizophrenia poses an evolutionary-genetic paradox because it exhibits strongly negative fitness effects and high heritability, yet it persists at a prevalence of approximately 1% across all human cultures. Recent theory has proposed a resolution: that genetic liability to schizophrenia has evolved as a secondary consequence of selection for human cognitive traits. This hypothesis predicts that genes increasing the risk of this disorder have been subject to positive selection in the evolutionary history of humans and other primates. We evaluated this prediction using tests for recent selective sweeps in human populations and maximum-likelihood tests for selection during primate evolution. Significant evidence for positive selection was evident using one or both methods for 28 of 76 genes demonstrated to mediate liability to schizophrenia, including DISC1, DTNBP1 and NRG1, which exhibit especially strong and well-replicated functional and genetic links to this disorder. Strong evidence of non-neutral, accelerated evolution was found for DISC1, particularly for exon 2, the only coding region within the schizophrenia-associated haplotype. Additionally, genes associated with schizophrenia exhibited a statistically significant enrichment in their signals of positive selection in HapMap and PAML analyses of evolution along the human lineage, when compared with a control set of genes involved in neuronal activities. The selective forces underlying adaptive evolution of these genes remain largely unknown, but these findings provide convergent evidence consistent with the hypothesis that schizophrenia represents, in part, a maladaptive by-product of adaptive changes during human evolution.

Molecular phylogenetic evidence for a mimetic radiation in Peruvian poison frogs supports a Müllerian mimicry hypothesis

Examples of Müllerian mimicry, in which resemblance between unpalatable species confers mutual benefit, are rare in vertebrates. Strong comparative evidence for mimicry is found when the colour and pattern of a single species closely resemble several different model species simultaneously in different geographical regions. Todemonstrate this, it is necessary to provide compelling evidence that the putative mimics do, in fact, form a monophyletic group. We present molecular phylogenetic evidence that the poison frog Dendrobates imitator mimics three different poison frogs in different geographical regions in Peru. DNA sequences from four different mitochondrial gene regions in putative members of a single species are analysed using parsimony, maximum-likelihood and neighbour-joining methods. The resulting hypotheses of phylogenetic relationships demonstrate that the different populations of D.imitator form a monophyletic group. To our knowledge, these results provide the first evidence for a Müllerian mimetic radiation in amphibians in which a single species mimics different sympatric species in different geographical regions.

A Key Ecological Trait Drove the Evolution of Biparental Care and Monogamy in an Amphibian

Linking specific ecological factors to the evolution of parental care pattern and mating system is a difficult task of key importance. We provide evidence from comparative analyses that an ecological factor (breeding pool size) is associated with the evolution of parental care across all frogs. We further show that the most intensive form of parental care (trophic egg feeding) evolved in concert with the use of small pools for tadpole deposition and that egg feeding was associated with the evolution of biparental care. Previous research on two Peruvian poison frogs (Ranitomeya imitator and Ranitomeya variabilis) revealed similar life histories, with the exception of breeding pool size. This key ecological difference led to divergence in parental care patterns and mating systems. We present ecological field experiments that demonstrate that biparental care is essential to tadpole survival in small (but not large) pools. Field observations demonstrate social monogamy in R. imitator, the species that uses small pools. Molecular analyses demonstrate genetic monogamy in R. imitator, the first example of genetic monogamy in an amphibian. In total, this evidence constitutes the most complete documentation to date that a single ecological factor drove the evolution of biparental care and genetic and social monogamy in an animal.

Parasitic exploitation as an engine of diversity

Parasitic exploitation occurs within and between a wide variety of taxa in a plethora of diverse contexts. Theoretical and empirical analyses indicate that parasitic exploitation can generate substantial genetic and phenotypic polymorphism within species. Under some circumstances, parasitic exploitation may also be an important factor causing reproductive isolation and promoting speciation. Here we review research relevant to the relationship between parasitic exploitation, within species‐polymorphism, and speciation in some of the major arenas in which such exploitation has been studied. This includes research on the vertebrate major histocompatibility loci, plant –pathogen interactions, the evolution of sexual reproduction, intragenomic conflict, sexual conflict, kin mimicry and social parasitism, tropical forest diversity and the evolution of language. We conclude by discussing some of the issues raised by comparing the effect of parasitic exploitation on polymorphism and speciation in different contexts.

Sexual selection and intra-femalecompetition in the green poison-dart frog, Dendrobates auratus

Observations on the mating and parental behaviour of the green poison-dart frog were used to test two hypotheses for the function of female-female competition in this species. The hypothesis that females compete to monopolize as many mates as possible was not supported because: (1) male territoriality was associated with competition for females; (2) intra-female competition for mates was not more common or intense than intra-male competition; (3) females were more selective about mating than were males; (4) estimated offspring production by individual females did not exceed the parental capacity of a single male. The hypothesis that females compete to monopolize the parental care of particular males was consistent with observations that: (I) females competed for males, but were more selective about mating than were males; (2) females remained near particular males and attempted to keep other females from mating with those males; (3) females may have used courtship to prevent males from mating with other females. Both hypotheses were consistent with evidence that: (I) females are large compared with males in D. auratus, relative to closely related species with low male parental investment; (2) females destroyed the eggs of other females when they located them. Williams (1966) and Trivers (1972) argued that relative parental investment is the primary determi- nant of the mating strategies of males and females in many species of animals. They argued that the sex that supplies the larger share of parental investment (investment in particular offspring that limits the parents potential to produce other offspring) will become a limiting resource for which members of the other sex compete. Females pro- vide most parental investment in most species that have been studied, and intra-male competition exceeds intra-female competition for mates, where- as females are often selective compared with males. In species where male parental investment signifi- cantly exceeds that of females, sex role reversal should occur, that is, females compete for a limited number of available males and males are choosier than females about whom they mate with. Citing observations of males performing parental care (Eaton 1941) and of more than one female follow- ing a single calling male (Dunn 1941), Trivers (1972) suggested that sex role reversal might occur in the green poison dart frog. Wells (I 978) studied D. auratus in the field and in captivity in Panama, and suggested that his observations were consistent with the hypothesis of sex role reversal; that small clutch size and large time investment by males in