SIGNALING EFFICACY DRIVES THE EVOLUTION OF LARGER SEXUAL ORNAMENTS BY SEXUAL SELECTION

Why are there so few small secondary sexual characters? Theoretical models predict that sexual selection should lead to reduction as often as exaggeration, and yet we mainly associate secondary sexual ornaments with exaggerated features such as the peacock's tail. We review the literature on mate choice experiments for evidence of reduced sexual traits. This shows that reduced ornamentation is effectively impossible in certain types of ornamental traits (behavioral, pheromonal, or color‐based traits, and morphological ornaments for which the natural selection optimum is no trait), but that there are many examples of morphological traits that would permit reduction. Yet small sexual traits are very rarely seen. We analyze a simple mathematical model of Fisher's runaway process (the null model for sexual selection). Our analysis shows that the imbalance cannot be wholly explained by larger ornaments being less costly than smaller ornaments, nor by preferences for larger ornaments being less costly than preferences for smaller ornaments. Instead, we suggest that asymmetry in signaling efficacy limits runaway to trait exaggeration.     

Female collared flycatchers learn to prefer males with an artificial novel ornament

We experimentally investigated whether learning from previousexperiences can lead to the establishment of a new mate preferencein a wild population of birds. During year one (2001), 63 femalecollared flycatchers (Ficedula albicollis) bred together withmales that we had provided with a novel trait, a red stripeon their white forehead patch (a sexually selected trait). Somecolor patterns of birds are largely determined by a few genes,and this experiment was designed to mimic the occurrence ofmutations in such genes. In the subsequent year (2002), we foundthat females with previous experience with red-striped maleswere more likely to pair with red-striped males (76%) than withcontrol males. By contrast, naïve females (i.e., with noprevious experience with red-striped males) were not more likelyto pair with red-striped males (44%) than with control males.Females paired with red-striped males produced more offspringthan females paired with control males, suggesting that maleswith the novel trait had become favored by selection. Thus,female collared flycatchers appear to quickly learn to associatea novel trait with a suitable mate that, in turn, leads to assortativemating between local mates (i.e., males with the new trait andfemales with previous experience of the new trait). Our resultsprovide support for the notion that learning may play an importantrole when the co-evolution of preferences and preferred traitstakes different routes in different populations of the samebird species.     

Heightened Condition Dependence of a Sexually Selected Signal in Male Polistes dominulus Paper Wasps

Sexually selected signals are theoretically expected to exhibit heightened condition dependence compared to non‐signaling traits. This link to condition enables sexual signals to provide information regarding individual quality and also provides a mechanism that allows animals to develop signals that accurately reflect their abilities. Most previous work on sexual signal condition dependence has focused on signals that have clear developmental costs, while less is known about the development of other types of quality signals. Male Polistes dominulus paper wasps have yellow‐on‐black abdominal spots that are important signals during female choice and male–male competition. These signals lack obvious production costs, as males are covered in yellow and black patterns composed of the same pigments. Here, we assess signal condition dependence by testing whether larval diet has a stronger influence on the development of male spots than on the development of control traits composed of the same pigments. Males reared on ad libitum diets developed elliptical spots similar to those seen on dominant, attractive males, while males reared on restricted diets developed irregularly shaped spots similar to those seen on subordinate, unattractive males. Remarkably, the development of a control trait composed of the same yellow and black pigments was not influenced by larval diet. Therefore, sexually selected signals can be developmentally decoupled from traits comprised of the same pigments. Condition dependence of sexually selected signals is likely to be a widespread solution to the challenge of developing sexually selected signals that accurately convey information about individual quality.     

Vicariance and convergence in Magellanic and New Zealand long‐looped brachiopod clades (Pan‐Brachiopoda: Terebratelloidea)

Phylogenetic reconstructions using parsimony, maximum likelihood (ML), and Bayesian relaxed molecular clock analyses of ～2850 nucleotides of nuclear‐encoded small and large subunit ribosomal DNAs (SSU and LSU rDNAs) from 14 long‐looped (terebratelloid) ingroup and four short‐looped (terebratulidine) outgroup brachiopod taxa, together with ML analyses of ～663 nucleotides of mitochondrial cytochrome oxidase subunit 1 (cox1) from 12 terebratelloid taxa, show that deep divergence separates taxa endemic to waters in the vicinity of New Zealand from those with a Magellanic distribution around South America and Antarctica. This deep divergence also separates Magellanic Terebratella dorsata from New Zealand Terebratella sanguinea, showing that they are not congeneric. Instead, they belong to separate ‘Magellanic’ (MAG) and ‘New Zealand’ (NZ) clades that first diverged about 82 Mya (95% highest posterior density, 48–120 Mya), correlating with separation between the NZ and Antarctic tectonic plates. Sequence analyses also reveal (1) that the Antarctic endemic taxa Magellania fragilis and Magellania joubini are not congeneric with Magellania venosa, suggesting that their previous placement in Aerothyris should be restored, and (2) that divergence between Antarctic and NZ species of the terebratulide Liothyrella occurred much later than plate separation, perhaps because of continuing gene flow caused by long‐lived larvae. The topology of the rDNA and cox1 gene trees implies that radial ornament of the shell (‘ribbing’) has been gained (and/or lost) independently within the MAG and NZ clades. Radial ribs are widespread in articulate brachiopods throughout the Phanerozoic, but no comparisons of brachiopod rib morphology and morphogenesis have been published. Our comparisons of transverse shell mid‐sections in the scanning electron microscope reveal no obvious evidence of differences in morphology between independently gained ribs. We also consider several ways in which ribs may affect fitness, including effects on hydrodynamics. Only scanty and inconclusive evidence is available, but we suggest that effects (if any) are likely to be of small magnitude; adaptive value of brachiopod shell ribs remains to be demonstrated. © 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 162 , 631–645.     

QTL linkage mapping of zebra finch beak color shows an oligogenic control of a sexually selected trait

Mate choice based on sexual ornaments can impose strong selection, which raises the question of how genetic variation in ornaments is maintained. One mechanism that has been proposed is genic capture. If ornament expression is influenced by general condition and condition is under polygenic control, selection will be inefficient in removing genetic variation. Here we analyze whether the genetic architecture of beak color in a population of zebra finches supports this hypothesis. Zebra finch beak color is commonly assumed to be under strong selection by mate choice, although some of the evidence is ambiguous. We show that beak redness has a heritability of 34% in our population and that it is strongly genetically correlated between the sexes, suggesting that it is largely controlled by the same genes in males and females. We mapped variation in beak redness based on 1404 single-nucleotide polymorphism (SNP) markers genotyped in a large pedigree. We find evidence for linkage on four chromosomes (Tgu1, Tgu5, Tgu13, Tgu21), which together explain a large part of the additive genetic variance. Our finding of genomic regions with major additive effects is not consistent with directional selection and genic capture, but rather suggests a role of antagonistic pleiotropy in maintaining genetic variation.     

Testosterone levels and gular pouch coloration in courting magnificent frigatebird (Fregata magnificens): variation with age-class, visited status and blood parasite infection

Male magnificent frigatebirds (Fregata magnificens) possess a seasonally expressed skin ornament, namely the red and inflatable gular pouch, and are, therefore, a convenient model for the study of some theories related to the evolution of possible testosterone-dependent sexual skin coloration. Here we report the findings of a study performed over four consecutive mating seasons in the Mexican national park Isla Isabel. We investigated differences in testosterone level and gular pouch coloration in courting males in relation to the categories: age-class, visited status and blood parasite infection. Gular pouch color saturation increased with age-class. Investigated frigatebirds were infected only with Haemoproteus iwa (Haemosporida, Haemoproteidae), with an overall prevalence infection of 15.5%. Prevalence of the infection increased with birds' age-class. Testosterone levels were significantly higher in infected males, who also had lighter colored gular pouches. In non-infected males, those visited by a female had higher testosterone levels than non-visited males. Gular pouch lightness and redness were negatively correlated but only redness in non-visited non-infected males was positively correlated with testosterone levels. Gular pouch saturation in visited and infected males was positively correlated with body mass, which also increased with age-class. Mated males had lower testosterone levels and lighter, less red and saturated gular pouch coloration than courting males. In summary, we found that coloration of the male skin ornament could reflect age-class (saturation), parasite infection (lightness) and mated status (all), together with indications of condition and testosterone dependency of ornament expression.     

Limits to environmental masking of genetic quality in sexual signals

There is considerable debate over the value of male sexual ornaments as signals of genetic quality. Studies alternately report that environmental variation enhances or diminishes the genetic signal, or leads to crossover where genotypes perform well in one environment but poorly in another. A unified understanding is lacking. We conduct a novel experimental test examining the dual effects of distinct categories of genetic (inbred vs. crossed parental lines) and environmental quality (low, through high to extreme larval food stress) on a condition‐dependent male ornament. We find that differences in genetic quality signalled by the ornament (male eyespan in Diasemopsis meigenii stalk‐eyed flies) become visible and are amplified under high stress but are overwhelmed in extreme‐stress environments. Variance among independent genetic lines increases with environmental stress in both genetic quality classes, but at a slower rate in high quality outcrossed flies. Individual genetic lines generally maintain their ranks across environments, except among high quality lines under low environmental stress, where low genetic variance among lines precludes differentiation between ranks. Our results provide a conceptual advance, demonstrating a unified pattern for how genetic and environmental quality interact. They show when environmental conditions lead to the amplification of differences in signals of genetic quality and thereby enhance the potential indirect genetic benefits gained by female mate choice.