A comparative study of phenotypic traits related to resource utilization in anuran communities

Larval anuran communities vary along a gradient of pond permanency. The families Hylidae, Ranidae, and Bufonidae have each diversified into multiple pond types. Species using ponds that dry seasonally (vernal ponds) must compete well to metamorphose before pond drying, while permanent ponds, which contain more predators, produce weaker selection for competitive ability. Quantifying phenotypic traits related to resource acquisition in 14 anuran species provides insight into the mechanistic underpinnings of adaptive radiation in anuran lineages. Under controlled laboratory conditions and at both early and late developmental stages, relative growth rate, relative consumption rate, assimilation efficiency and production efficiency varied significantly among species. As predicted, vernal pond species had high growth rates relative to species using more than one pond type. However, within a pond type, families frequently differed in phenotype. In species using permanent ponds with fish predators, hylids had high growth rates while ranids had low growth rates, and in species using vernal ponds, bufonids had higher assimilation efficiencies than hylids. Differences also occurred between stages; hylids and ranids in permanent, but fishless, ponds were similar at an early stage, but late stage hylids in the same pond type had lower growth and consumption rates, and higher assimilation efficiencies than ranids. Functional relationships between phenotypic traits also differed among species and developmental stage. Negative correlations between evolutionary change (independent contrast values) in both mass and growth rate (both stages), and mass and consumption rate (late stage), suggest the presence of trade-offs. These results indicate that different lineages have diversified in different ways into the same pond types.     

Evolutionary Patterns in Advanced Snakes

One prevalent view of phylogenetic events in advanced snakesholds that the fangs evolved along at least two pathways one(e.g. elapids) from ancestors with enlarged anterior and theother (e.g. viperids) from ancestors with enlarged posteriormaxillary teeth. Selective forces driving these changes arepresumed to arise from the increasing advantages of teeth andglands in venom injection. In this paper another plausible viewof these events is proposed. First fangs of both elapids and viperids likely evolved fromreal maxillary teeth. In non-venomous snakes, differences intooth morphology and function suggest that there may be somedivision of labor among anterior and posterior maxillary teeth.Anterior maxillary teeth, residing forward in the mouth likelyserve the biological role of snaring and impaling prey duringthe strike. They are also conical frequently recurved and lacka secretion groove. On the other hand posterior teeth becauseof their geometric position on the maxilla and mechanical advantages,tend to serve as aids in preingestion manipulation and swallowingof prey. They are often blade shaped and occasionally bear asecretion groove along their sides. Although both front andrear maxillary teeth of nonvenomous snakes may be elongatedthis is likely to serve these different functional roles andhence they evolved under different selective pressures. Whenfangs evolved they did so several times independently but fromrear maxillary teeth. In support one notes a) the similar positionpostorbital of venom and Duvernoy s glands b) similar embryonicdevelopment of fangs and rear maxillary teeth c) secretion groovewhen present, is found only on rear teeth and d) similar biologicalroles of some rear teeth and fangs. For ease in clearance ofthe prey during the strike the fangs are positioned forwardin the mouth accomplished in viperid snakes by forward rotationof the maxilla and elapids by rostral anatomical migration tothe front of the maxilla. Second, the adaptive advantage first favoring initial rear toothenlargement likely centered not on their role in venom injectionbut rather on their role in preingestion manipulation and swallowing.However once enlarged, teeth would be preadapted for later modificationinto fangs under selection pressures arising from advantagesof venom introduction. This has implications for the function and evolution of associatedstructures. Besides possibly subduring or even killing of preythe secretion of Duvernoy's gland may be involved in digestionor in neutralizing noxious or fouling products of the prey.The presence or absence of constriction need not be functionallytied to absence or presence of venom injection. The phylogeneticpathways outlined herein were likely traveled several timesindependently in advanced snakes.     

Intraspecific variation in advertisement call characteristics and acoustic strategies among male forest green tree frogs

Frogs are a representative taxon that use advertisement calls to aid in reproduction. In most frog species, calls vary with body size, and allometric constraints between body size and call frequency have been widely reported among anuran species. Although this variation is an important driver of sexual selection in frogs, male advertisement call strategies may also vary according to body size. In this study, we conducted playback experiments on the male forest green tree frog (Zhangixalus arboreus) to determine whether male advertisement call characteristics and strategies vary according to body size and the amplitude of intraspecific chorus noise. The results indicated that the calls of larger individuals are louder and lower than those of smaller ones, who call more frequently; moreover, the calls become lower, and the number of calls decreases, as noise levels increase. These findings suggest that forest green tree frog emits lower calls or refrains from calling when chorus noise increases, and that intraspecific variation in advertisement call characteristics can induce different strategies in response to chorus noise. Because advertisement call variation with body size is common among frog species, intraspecific variation in male advertisement call strategies may also be a common phenomenon.     

Antagonism between sexual and natural selection in experimental populations of Saccharomyces cerevisiae

Trade-offs between life-history components are a central concept of evolution and ecology. Sexual and natural selection seem particularly apt to impose antagonistic selective pressures. When sex is not integrated into reproduction, as in Saccharomyces cerevisiae, natural selection can impair or even eliminate it. In this study, a genetic trade-off between the sexual and asexual phases of the yeast life cycle was suggested by sharp declines in the mating and sporulation abilities of unrelated genotypes that were propagated asexually in minimal growth medium and in mice. When sexual selection was applied to populations that had previously evolved asexually, sexual fitness increased but asexual fitness declined. No such negative correlation was observed when sexual selection was applied to an ancestral strain: sexual and asexual fitness both increased. Thus, evolutionary history affected the evolution of genetic correlations, as fitness increases in a population already well adapted to the environment were more likely to come at the expense of sexual functions.     

Sexual dimorphism in the tusked frog, Adelotus brevis (Anura:Myobatrachidae): the roles of natural and sexual selection

At least two adaptive processes can lead to the evolution of sexual dimorphism: sexual selection (e.g. male-male combat) or natural selection (e.g. dietary divergence). We investigated the adaptive significance of a distinctive pattern of sexual dimorphism in a south-eastern Australian frog, Adelotus brevis. Male Adelotus grow larger than female conspecifics, have larger heads relative to body size, and have large paired projections (‘tusks’) in the lower jaw. All of these traits are rare among anurans. We quantified the degree of dimorphism in Adelotus, and gathered data on diets and mating systems of this species to evaluate the possible roles of sexual selection and dietary divergence in favoring die evolution of these sexually dimorphic traits. Analysis of prey items in alimentary tracts revealed significant sex differences in prey types. For example, females ate proportionally more arthropods and fewer molluscs than did males. However, this difference is likely to be a secondary consequence of habitat differences between the sexes (due in turn to their different reproductive roles) rather than a selective force for the evolution of sexual dimorphism. Calling males spend their time in moist habitats where pondsnails are abundant, whereas females are more often encountered in the drier arthropod-rich woodlands. A three-year behavioural ecology study on a field population revealed that reproductive males engage in agonistic interactions, with the sexually dimorphic tusks used to attack rivals. Larger body size contributed to male reproductive success. Small males were excluded from calling sites and, among the calling males, larger animals had higher reproductive success (numbers of matings) than did smaller individuals. Hence, the atypical pattern of sexual dimorphism in Adelotus brevis seems to have resulted from sexual selection for larger body size and tusk size in males, in the context of male-male agonistic behaviour, rather than natural selection for ecological divergence between the sexes.     

Male secondary sexual characteristics, sexual selection, and molecular divergence in fanged ranid frogs of Southeast Asia

A group of Southeast Asian frogs of the family Ranidae are characterized by a suite of unusual secondary sexual characteristics. Males are larger than females, possess bony odontoid processes (fangs) and have enlarged heads. While all members of this clade are sexually dimorphic in this suite of characters, the degree of development of the secondary sexual characteristics in males varies widely across species. One of the most common species, Rana blythii Boulenger, has an extremely broad geographical range. This frog lacks an advertisement call in Borneo but calling has been reported in populations from peninsular Malaysia and Vietnam. This study examines the relationship between the expression of male secondary sexual characteristics, molecular divergence and number of speciation events in widely separated populations of R. blythii , and between R. blythii and other species of closely related fanged frogs belonging to the grunniens species group. Results from morphometric and sequence data indicate that (1) there is no correlation between morphological and molecular distance in these frogs and (2) there is no correlation between morphological distance and the number of speciation events separating taxa. Systematic analysis demonstrates that R. blythii , as currently recognized, is not a single species nor is it monophyletic.     

Sexual and natural selection in the evolution of extended phenotypes: the use of green nesting material in starlings

Although sexual selection is typically considered the predominant force driving the evolution of ritualized sexual behaviours, natural selection may also play an important and often underappreciated role. The use of green aromatic plants among nesting birds has been interpreted as a component of extended phenotype that evolved either via natural selection due to potential sanitary functions or via sexual selection as a signal of male attractiveness. Here, we compared both hypotheses using comparative methods in starlings, a group where this behaviour is widespread. We found that the use of green plants was positively related to male‐biased size dimorphism and that it was most likely to occur among cavity‐nesting species. These results suggest that this behaviour is likely favoured by sexual selection, but also related to its sanitary use in response to higher parasite loads in cavities. We speculate that the use of green plants in starlings may be facilitated by cavity nesting and was subsequently co‐opted as a sexual signal by males. Our results represent an example of how an extended phenotypic component of males becomes sexually selected by females. Thus, both natural selection and sexual selection are necessary to fully understand the evolution of ritualized behaviours involved in courtship.     

Field Response of Tadpoles to Conspecific and Heterospecific Alarm

Many organisms use chemical cues from a variety of sources to mediate predator avoidance. Response to heterospecific alarm cues has been demonstrated for tadpoles within but not among taxa and alarm response behavior has seldom been examined under field conditions. This study examined the response of three sympatric amphibian larvae and predaceous larval Dytiscus sp. (diving beetle) to damage-release signals in natural ponds by using capture rates from treated funnel traps as an index of larval behavior. Hyla regilla (Pacific tree frog) tadpoles avoided traps treated with either crushed conspecifics or with Rana aurora (red-legged frog) tadpoles but the larger ranids and Ambystoma macrodactylum (long-toed salamander) did not respond to either treatment. H. regilla tadpoles were likely susceptible to any potential predators of ranid tadpoles in these ponds and this result is consistent with the hypothesis that a response to heterospecific alarm occurs in sympatric prey with shared predators.     

Migration and the evolution of sexual dichromatism: evolutionary loss of female coloration with migration among wood-warblers

The mechanisms underlying evolutionary changes in sexual dimorphism have long been of interest to biologists. A striking gradient in sexual dichromatism exists among songbirds in North America, including the wood-warblers (Parulidae): males are generally more colourful than females at northern latitudes, while the sexes are similarly ornamented at lower latitudes. We use phylogenetically controlled comparative analysis to test three non-mutually exclusive hypotheses for the evolution of sexual dichromatism among wood-warblers. The first two hypotheses focus on the loss of female coloration with the evolution of migration, either owing to the costs imposed by visual predators during migration, or owing to the relaxation of selection for female social signalling at higher latitudes. The third hypothesis focuses on whether sexual dichromatism evolved owing to changes in male ornamentation as the strength of sexual selection increases with breeding latitude. To test these hypotheses, we compared sexual dichromatism to three variables: the presence of migration, migration distance, and breeding latitude. We found that the presence of migration and migration distance were both positively correlated with sexual dichromatism, but models including breeding latitude alone were not strongly supported. Ancestral state reconstruction supports the hypothesis that the ancestral wood-warblers were monochromatic, with both colourful males and females. Combined, these results are consistent with the hypotheses that the evolution of migration is associated with the relaxation of selection for social signalling among females and that there are increased predatory costs along longer migratory routes for colourful females. These results suggest that loss of female ornamentation can be a driver of sexual dichromatism and that social or natural selection may be a stronger contributor to variation in dichromatism than sexual selection.     

Sexually selected females in the monogamous Western Australian seahorse

Studies of sexual selection in monogamous species have hitherto focused on sexual selection among males. Here, we provide empirical documentation that sexual selection can also act strongly on females in a natural population with a monogamous mating system. In our field-based genetic study of the monogamous Western Australian seahorse, Hippocampus subelongatus, sexual selection differentials and gradients show that females are under stronger sexual selection than males: mated females are larger than unmated ones, whereas mated and unmated males do not differ in size. In addition, the opportunity for sexual selection (variance in mating success divided by its mean squared) for females is almost three times that for males. These results, which seem to be generated by a combination of a male preference for larger females and a female-biased adult sex ratio, indicate that substantial sexual selection on females is a potentially important but under-appreciated evolutionary phenomenon in monogamous species.     

Integumentary structure and its relationship to wiping behaviour in the common Indian tree frog, Polypedates maculatus

Skin of the Indian tree frog, Polypedates maculatus (Rhacophoridae), was studied in the context of self-wiping behaviour which functions to expel and distribute cutaneous secretions recently shown to retard evaporative water loss. The secretions contain both mucus and lipids and are derived from a common gland considered to be homologous with characteristic anuran mucous glands. The glands are bipotent and secrete both mucus and lipoid products which are evidently mixed within the glandular lumen. Another type of gland resembling characteristic anuran serous (or granular) glands is found in dorsal but not ventral skin, whereas the lipid-secreting mucous glands are found in skin associated with all body surfaces. There is no distinct, lipid-secreting gland present in the skin of this species other than the mucous glands. These histochemical data complement the earlier finding that resistance to evaporative water loss in this species is relatively small compared with phyllomedusine 'waterproof frogs which also exhibit wiping behaviour associated with secretion of lipids. Thus, wiping behaviour may have evolved in association with mucous secretions before dominant lipoid secretions resulted from strong selection for water conservation.     

Comparison of cranial form and function in association with diet in natricine snakes

The skull of squamates has many functions, with food acquisition and ingestion being paramount. Snakes vary interspecifically in the frequency, size, and types of prey that are consumed. Natural selection should favor phenotypes that minimize the costs of energy acquisition; therefore, trophic morphology should reflect a snake's primary prey type to enhance some aspect of feeding performance. I measured 19 cranial variables for six natricine species that vary in the frequency with which they consume frogs and fish. Both conventional and phylogenetically corrected analyses indicated that fish‐eating snakes have relatively longer upper and lower jaw elements than frog‐eating snakes, which tended to have broader skull components. I also compared the ratio of the in‐lever to the out‐lever lengths of the jaw‐closing mechanism [jaw mechanical advantage (MA)] among species. Fish‐eating snakes had significantly lower MAs in the jaws than did the frog‐eating snakes. This result suggests that piscivores have faster closing jaws and that the jaws of frog‐eating snakes have higher closing forces. Cranial morphology and the functional demands of prey capture and ingestion appear to be associated with primary prey type in natricine snakes. J. Morphol., 2011. © 2011 Wiley‐Liss, Inc.     

Antagonistic responses to natural and sexual selection and the sex-specific evolution of cuticular hydrocarbons in Drosophila simulans

Natural and sexual selection are classically thought to oppose one another, and although there is evidence for this, direct experimental demonstrations of this antagonism are largely lacking. Here, we assessed the effects of sexual and natural selection on the evolution of cuticular hydrocarbons (CHCs), a character subject to both modes of selection, in Drosophila simulans. Natural selection and sexual selection were manipulated in a fully factorial design, and after 27 generations of experimental evolution, the responses of male and female CHCs were assessed. The effects of natural and sexual selection differed greatly across the sexes. The responses of female CHCs were generally small, but CHCs evolved predominantly in the direction of natural selection. For males, profiles evolved via sexual and natural selection, as well as through the interaction between the two, with some male CHC components only evolving in the direction of natural selection when sexual selection was relaxed. These results indicate sex‐specific responses to selection, and that sexual and natural selection act antagonistically for at least some combinations of CHCs.     

Cranial ontogeny in Philautus silus (Anura: Ranidae: Rhacophorinae) reveals few similarities with other direct-developing anurans

Direct development has evolved in rhacophorine frogs independently from other anuran lineages, thereby offering an opportunity to assess features associated with this derived life history. Using a developmental series of the direct-developing Philautus silus (Ranidae: Rhacophorinae) from Sri Lanka, we examine features of cranial morphology that are part of a suite of adaptations that facilitate feeding in free-living tadpoles, but have been changed or lost in other direct-developing lineages. Larval-specific upper jaw cartilages, which are absent from many non-rhacophorine direct-developing species (such as Eleutherodactylus coqui), develop in embryos of P. silus. Similarly, lower jaw cartilages initially assume a larval morphology, which is subsequently remodeled into the adult jaw configuration before hatching. However, the cartilaginous jaw suspension and hyobranchial skeleton never assume a typical larval morphology. The palatoquadrate, which suspends the lower jaw, lacks the posterior connections to the braincase found in many metamorphosing species. Unlike in metamorphosing species, bone formation in P. silus begins before hatching. However, the sequence of bone formation resembles that of metamorphosing anurans more than that of other direct developers. In particular, P. silus does not exhibit precocious ossification of the lower jaw, which is characteristic of some frogs and caecilians that lack a free-living tadpole. These data reveal some similarities between Philautus and other direct-developing anurans. However, the departure of Philautus embryos from the generalized tadpole skeletal morphology is less pronounced than that observed in other direct-developing taxa.     

Interaction between natural and sexual selection during the evolution of mate recognition

The interaction between natural and sexual selection is central to many theories of how mate choice and reproductive isolation evolve, but their joint effect on the evolution of mate recognition has not, to my knowledge, been investigated in an evolutionary experiment. Natural and sexual selection were manipulated in interspecific hybrid populations of Drosophila to determine their effects on the evolution of a mate recognition system comprised of cuticular hydrocarbons (CHCs). The effect of natural selection in isolation indicated that CHCs were costly for males and females to produce. The effect of sexual selection in isolation indicated that females preferred males with a particular CHC composition. However, the interaction between natural and sexual selection had a greater effect on the evolution of the mate recognition system than either process in isolation. When natural and sexual selection were permitted to operate in combination, male CHCs became exaggerated to a greater extent than in the presence of sexual selection alone, and female CHCs evolved against the direction of natural selection. This experiment demonstrated that the interaction between natural and sexual selection is critical in determining the direction and magnitude of the evolutionary response of the mate recognition system.     

Population density and structure drive differential investment in pre‐ and postmating sexual traits in frogs

Sexual selection theory predicts a trade‐off between premating (ornaments and armaments) and postmating (testes and ejaculates) sexual traits, assuming that growing and maintaining these traits is costly and that total reproductive investments are limited. The number of males in competition, the reproductive gains from investing in premating sexual traits, and the level of sperm competition are all predicted to influence how males allocate their finite resources to these traits. Yet, empirical examination of these predictions is currently scarce. Here, we studied relative expenditure on pre‐ and postmating sexual traits among frog species varying in their population density, operational sex ratio, and the number of competing males for each clutch of eggs. We found that the intensifying struggle to monopolize fertilizations as more and more males clasp the same female to fertilize her eggs shifts male reproductive investment toward sperm production and away from male weaponry. This shift, which is mediated by population density and the associated level of male–male competition, likely also explains the trade‐off between pre‐ and postmating sexual traits in our much broader sample of anuran species. Our results highlight the power of such a multilevel approach in resolving the evolution of traits and allocation trade‐offs.     

Sexual selection impacts brain anatomy in frogs and toads

Natural selection is a major force in the evolution of vertebrate brain size, but the role of sexual selection in brain size evolution remains enigmatic. At least two opposing schools of thought predict a relationship between sexual selection and brain size. Sexual selection should facilitate the evolution of larger brains because better cognitive abilities may aid the competition for mates. However, it may also restrict brain size evolution due to energetic trade‐offs between brain tissue and sexually selected traits. Here, we examined the patterns of selection on brain size and brain anatomy in male anurans (frogs and toads), a group where the strength of sexual selection differs markedly among species, using a phylogenetically controlled generalized least‐squared (PGLS) regression analyses. The analysis revealed that in 43 Chinese anuran species, neither mating system, nor type of courtship, or testes mass was significantly associated with relative brain size. While none of those factors related to the relative size of olfactory nerves, optic tecta, telencephalon, and cerebellum, the olfactory bulbs were relatively larger in monogamous species and those using calls during courtship. Our findings support the mosaic model of brain evolution and suggest that while the investigated aspects of sexual selection do not seem to play a prominent role in the evolution of brain size of anurans, they do impact their brain anatomy.     

Molecular strategies in biological evolution of antimicrobial peptides

Gene-encoded antimicrobial peptides that protect the skin of hylid and ranin frogs against noxious microorganisms are processed from a unique family of precursor polypeptides with a unique pattern of conserved and variable regions opposite to that of conventional secreted peptides. Precursors belonging to this family, designated the preprodermaseptin, have a common N-terminal preproregion that is remarkably well conserved both within and between species, but a hypervariable C-terminal domain corresponding to antimicrobial peptides with very different lengths, sequences, charges and antimicrobial spectra. Each frog species has its own distinct panoply of 10-20 antimicrobial peptides so that the 5000 species of ranids and hylids may produce approximately 100,000 different peptide antibiotics. The strategy that these frogs have evolved to generate this enormous array of peptides includes repeated duplications of a 150 million years old ancestral gene, focal hypermutation of the antimicrobial peptide domain maybe involving a mutagenic DNA polymerase similar to Escherichia coli Pol V, and subsequent actions of positive (diversifying) selection. The hyperdivergence of skin antimicrobial peptides can be viewed as the successful evolution of a multi-drug defense system that provides frogs with maximum protection against rapidly changing microbial biota and minimizes the chance of microorganisms developing resistance to individual peptides. The impressive variations in the expression of frog skin antimicrobial peptides may be exploited for discovering new molecules and structural motifs targeting specific microorganisms for which the therapeutic armamentarium is scarce.