Sex-specific plasticity and genotype × sex interactions for age and size of maturity in the sheepshead swordtail, Xiphophorus birchmanni.

Responses to sexually antagonistic selection are thought to be constrained by the shared genetic architecture of homologous male and female traits. Accordingly, adaptive sexual dimorphism depends on mechanisms such as genotype-by-sex interaction (G×S) and sex-specific plasticity to alleviate this constraint. We tested these mechanisms in a population of Xiphophorus birchmanni (sheepshead swordtail), where the intensity of male competition is expected to mediate intersexual conflict over age and size at maturity. Combining quantitative genetics with density manipulations and analysis of sex ratio variation, we confirm that maturation traits are dimorphic and heritable, but also subject to large G×S. Although cross-sex genetic correlations are close to zero, suggesting sex-linked genes with important effects on growth and maturation are likely segregating in this population, we found less evidence of sex-specific adaptive plasticity. At high density, there was a weak trend towards later and smaller maturation in both sexes. Effects of sex ratio were stronger and putatively adaptive in males but not in females. Males delay maturation in the presence of mature rivals, resulting in larger adult size with subsequent benefit to competitive ability. However, females also delay maturation in male-biased groups, incurring a loss of reproductive lifespan without apparent benefit. Thus, in highly competitive environments, female fitness may be limited by the lack of sex-specific plasticity. More generally, assuming that selection does act antagonistically on male and female maturation traits in the wild, our results demonstrate that genetic architecture of homologous traits can ease a major constraint on the evolution of adaptive dimorphism.

Physiological adaptation along environmental gradients and replicated hybrid zone structure in swordtails (Teleostei: Xiphophorus).

Local adaptation is often invoked to explain hybrid zone structure, but empirical evidence of this is generally rare. Hybrid zones between two poeciliid fishes, Xiphophorus birchmanni and X. malinche, occur in multiple tributaries with independent replication of upstream-to-downstream gradients in morphology and allele frequencies. Ecological niche modelling revealed that temperature is a central predictive factor in the spatial distribution of pure parental species and their hybrids and explains spatial and temporal variation in the frequency of neutral genetic markers in hybrid populations. Among populations of parentals and hybrids, both thermal tolerance and heat-shock protein expression vary strongly, indicating that spatial and temporal structure is likely driven by adaptation to local thermal environments. Therefore, hybrid zone structure is strongly influenced by interspecific differences in physiological mechanisms for coping with the thermal environment.

Replicated hybrid zones of Xiphophorus swordtails along an elevational gradient.

Natural hybrid zones provide opportunities to study a range of evolutionary phenomena from speciation to the genetic basis of fitness-related traits. We show that widespread hybridization has occurred between two neo-tropical stream fishes with partial reproductive isolation. Phylogenetic analyses of mitochondrial sequence data showed that the swordtail fish Xiphophorus birchmanni is monophyletic and that X. malinche is part of an independent monophyletic clade with other species. Using informative single nucleotide polymorphisms in one mitochondrial and three nuclear intron loci, we genotyped 776 specimens collected from twenty-three sites along seven separate stream reaches. Hybrid zones occurred in replicated fashion in all stream reaches along a gradient from high to low elevation. Genotyping revealed substantial variation in parental and hybrid frequencies among localities. Tests of F(IS) and linkage disequilibrium (LD) revealed generally low F(IS) and LD except in five populations where both parental species and hybrids were found suggesting incomplete reproductive isolation. In these locations, heterozygote deficiency and LD were high, which suggests either selection against early generation hybrids or assortative mating. These data lay the foundation to study the adaptive basis of the replicated hybrid zone structure and for future integration of behaviour and genetics to determine the processes that lead to the population genetic patterns observed in these hybrid zones.

An indigenous religious ritual selects for resistance to a toxicant in a livebearing fish.

Human-induced environmental change can affect the evolutionary trajectory of populations. In Mexico, indigenous Zoque people annually introduce barbasco, a fish toxicant, into the Cueva del Azufre to harvest fish during a religious ceremony. Here, we investigated tolerance to barbasco in fish from sites exposed and unexposed to the ritual. We found that barbasco tolerance increases with body size and differs between the sexes. Furthermore, fish from sites exposed to the ceremony had a significantly higher tolerance. Consequently, the annual ceremony may not only affect population structure and gene flow among habitat types, but the increased tolerance in exposed fish may indicate adaptation to human cultural practices in a natural population on a very small spatial scale.

The shape of things to come: linking developmental plasticity to post-metamorphic morphology in anurans.

Development consists of growth and differentiation, which can be partially decoupled and can be affected by environmental factors to different extents. In amphibians, variation in the larval environment influences development and causes changes in post-metamorphic shape. We examined post-metamorphic consequences, both morphological and locomotory, of alterations in growth and development. We reared tadpoles of two phylogenetically and ecologically distant frog species (the red-eyed treefrog Agalychnis callidryas and the African clawed frog Xenopus laevis) under different temperatures with ad libitum food supply and under different food levels at a constant temperature. Low temperature and low food levels both resulted in similarly extended larval periods. However, low temperature yielded relatively long-legged frogs with a lower degree of ossification than warm temperature, whereas low food yielded relatively short-legged frogs with a higher degree of ossification than high food levels. Such allometric differences had no effect on locomotor performance of juveniles. Our results provide a basis for understanding the relationship between growth, differentiation and post-metamorphic shape in anurans and help explain many of the discrepancies reported in previous studies.

Shared preferences by predators and females for male ornaments in swordtails.

Sexually dimorphic traits in many mate recognition systems have evolved in response to preexisting female biases. These biases are often quite general in form and are likely to be shared by predators, thereby imposing a cost on male trait expression. The Mexican tetra Astyanax mexicanus (Pisces: Characidae), a visual predator of swordtail fishes, exhibits the same visual preferences for male body size morphs as do females. Furthermore, tetras in populations where swordtails are absent prefer males with sword ornaments over males with swords removed. The predator preference is thus likely to have arisen prior to contact with fishes bearing the ornament, as has also been suggested for mating preferences for swords.

Visual and acoustic communication in non-human animals: a comparison.

The visual and auditory systems are two major sensory modalities employed in communication. Although communication in these two sensory modalities can serve analogous functions and evolve in response to similar selection forces, the two systems also operate under different constraints imposed by the environment and the degree to which these sensory modalities are recruited for non-communication functions. Also, the research traditions in each tend to differ, with studies of mechanisms of acoustic communication tending to take a more reductionist tack often concentrating on single signal parameters, and studies of visual communication tending to be more concerned with multivariate signal arrays in natural environments and higher level processing of such signals. Each research tradition would benefit by being more expansive in its approach.

Female preference for swords in Xiphophorus helleri reflects a bias for large apparent size.

Swordtail fish (Poeciliidae: genus Xiphophorus) are a paradigmatic case of sexual selection by sensory exploitation. Female preference for males with a conspicuous "sword" ornament is ancestral, suggesting that male morphology has evolved in response to a preexisting bias. The perceptual mechanisms underlying female mate choice have not been identified, complicating efforts to understand the selection pressures acting on ornament design. We consider two alternative models of receiver behavior, each consistent with previous results. Females could respond either to specific characteristics of the sword or to more general cues, such as the apparent size of potential mates. We showed female swordtails a series of computer-altered video sequences depicting a courting male. Footage of an intact male was preferred strongly to otherwise identical sequences in which portions of the sword had been deleted selectively, but a disembodied courting sword was less attractive than an intact male. There was no difference between responses to an isolated sword and to a swordless male of comparable length, or between an isolated sword and a homogenous background. Female preference for a sworded male was abolished by enlarging the image of a swordless male to compensate for the reduction in length caused by removing the ornament. This pattern of results is consistent with mate choice being mediated by a general preference for large males rather than by specific characters. Similar processes may account for the evolution of exaggerated traits in other systems.