Species divergence in sexually selected traits: increase in song elaboration is related to decrease in plumage ornamentation in finches

Elaborate plumage and complex songs of male birds are two of the best-known examples of sexually selected traits, yet the interaction between these traits is poorly understood. Theory suggests that among a suite of potential displays, animals will emphasize traits that are most conspicuous, least costly, or best signal condition and reduce display of other traits. Here we examined the relationship between song and plumage elaborations in cardueline finches, songbirds that are highly variable in plumage displays and songs, but that share a similar mating system. We statistically controlled for body mass, habitat characteristics, and phylogenetic relationships and found that across species song complexity was strongly negatively related to elaboration of plumage ornamentation. When plumage coloration was partitioned into carotenoid-based and melanin-based components, song complexity was negatively related to elaboration of male carotenoid-based coloration but unrelated to elaboration of melanin-based coloration. These observations support the idea that, for condition-dependent traits, animal species trade off trait expression in response to changes in the costs or the information content of these traits. We discuss several alternative explanations for the observed pattern.     

Multimodal signalling in the North American barn swallow: a phenotype network approach

Complex signals, involving multiple components within and across modalities, are common in animal communication. However, decomposing complex signals into traits and their interactions remains a fundamental challenge for studies of phenotype evolution. We apply a novel phenotype network approach for studying complex signal evolution in the North American barn swallow (Hirundo rustica erythrogaster). We integrate model testing with correlation-based phenotype networks to infer the contributions of female mate choice and male–male competition to the evolution of barn swallow communication. Overall, the best predictors of mate choice were distinct from those for competition, while moderate functional overlap suggests males and females use some of the same traits to assess potential mates and rivals. We interpret model results in the context of a network of traits, and suggest this approach allows researchers a more nuanced view of trait clustering patterns that informs new hypotheses about the evolution of communication systems.     

Differential rates of phenotypic introgression are associated with male behavioral responses to multiple signals

Sexual selection on multiple signals may lead to differential rates of signal introgression across hybrid zones if some signals contribute to reproductive isolation but others facilitate gene flow. Competition among males is one powerful form of sexual selection, but male behavioral responses to multiple traits have not been considered in a system where traits have introgressed differentially. Using playbacks, mounts, and a reciprocal experimental design, we tested the hypothesis that male responses to song and plumage in two subspecies of red‐backed fairy‐wren (Malurus melanocephalus) explain patterns of differential signal introgression (song has not introgressed, whereas plumage color has introgressed asymmetrically). We found that males of both subspecies discriminated symmetrically between subspecies’ songs at a long range, but at a close range, we found that aggression was equal for both subspecies’ plumage and songs. Taken together, our results suggest that male behavioral responses hinder the introgression of song, but allow for the observed asymmetrical introgression of plumage. Our results highlight how behavioral responses are a key component of signal evolution when recently divergent taxa come together, and how differential responses to multiple signals may lead to differential signal introgression and novel trait combinations.     

Condition-dependent traits and the capture of genetic variance in male advertisement song

The occurrence of additive genetic variance (VA) for male sexual traits remains a major problem in evolutionary biology. Directional selection normally imposed by female choice is expected to reduce VA greatly, yet recent surveys indicate that a substantial amount remains in many species. We addressed this problem, also known as the 'lek paradox', in Achroia grisella (Lepidoptera: Pyralidae), an acoustic moth in which males advertise to females with a pulsed ultrasonic song. Using a standard half-sib/full-sib breeding design, we generated F1 progeny from whom we determined VA and genetic covariance (COVA) among seven traits: three song characters, an overall index of song attractiveness, nightly singing period, adult lifespan, and body mass at adult eclosion. Because A. grisella neither feed nor drink as adults, the last trait, eclosion body mass, is considered a measure of 'condition'. We found significant levels of VA and narrow-sense heritabilities (h2) for all seven traits and significant genetic correlations (= COVAi,j / radical (VA i x VA j)) between most pairs of traits (i, j). Male attractiveness was positively correlated with body mass (condition), adult lifespan, and nightly singing period, which we interpret as an energy constraint preventing males in poor condition from singing attractively, from singing many hours per night, and from surviving an extended lifespan. The positive genetic correlation (r = 0.79) between condition and attractiveness, combined with significant levels of VA for both traits, indicates that much of the variation in male song can be explained by VA for condition. Finally, we discuss the morphological and physiological links between condition and song attractiveness, and the ultimate factors that may maintain VA for condition.     

Antagonistic pleiotropy in species with separate sexes,and the maintenance of genetic variation in life‐history traits and fitness

Antagonistic pleiotropy (AP)—where alleles of a gene increase some components of fitness at a cost to others—can generate balancing selection, and contribute to the maintenance of genetic variation in fitness traits, such as survival, fecundity, fertility, and mate competition. Previous theory suggests that AP is unlikely to maintain variation unless antagonistic selection is strong, or AP alleles exhibit pronounced differences in genetic dominance between the affected traits. We show that conditions for balancing selection under AP expand under the likely scenario that the strength of selection on each fitness component differs between the sexes. Our model also predicts that the vast majority of balanced polymorphisms have sexually antagonistic effects on total fitness, despite the absence of sexual antagonism for individual fitness components. We conclude that AP polymorphisms are less difficult to maintain than predicted by prior theory, even under our conservative assumption that selection on components of fitness is universally sexually concordant. We discuss implications for the maintenance of genetic variation, and for inferences of sexual antagonism that are based on sex‐specific phenotypic selection estimates—many of which are based on single fitness components.     

Evolutionary trade‐off between naturally‐ and sexually‐selected melanin‐based colour traits in worldwide barn owls and allies

Natural selection typically constrains the evolution of sexually‐selected characters. The evolution of naturally‐ and sexually‐selected traits can be intertwined if they share part of their genetic machinery or if sex traits impair foraging success or increase the risk of depredation. The present study investigated phenotypic correlations between naturally‐ and sexually‐selected plumage traits in the Tytonidae (barn owls, grass owls, and masked owls). Phenotypic correlations indicate the extent to which selection on one trait will indirectly influence the evolution of another trait. In this group of birds, the ventral body side varies from white to dark reddish, a naturally‐selected pheomelanin‐based colour trait with important roles in predator–prey interactions. Owls also exhibit eumelanin‐based black spots, for which number and size signal different aspects of individual quality and are used in mate choice. These three plumage traits are strongly heritable and sexually dimorphic, with females being on average darker reddish and more spotted than males. Phenotypic correlations were measured between these three plumage traits in 3958 free‐living barn owls in Switzerland and 10 670 skin specimens from 34 Tyto taxa preserved in museums. Across Tyto taxa, the sexually‐selected plumage spottiness was positively correlated with the naturally‐selected reddish coloration, with redder birds being more heavily spotted. This suggests that they are genetically constrained or that natural and sexual selection are not antagonistically exerted on plumage traits. In a large sample of Swiss nestlings and within 34 Tyto taxa, the three plumage traits were positively correlated. The production of melanin pigments for one plumage trait is therefore not traded off against the production of melanin pigments for another plumage trait. Only in the most heavily‐spotted Tyto taxa do larger‐spotted individuals display fewer spots. This indicates that, at some threshold value, the evolution of many spots constrains the evolution of large spots. These analyses raise the possibility that different combinations of melanin‐based plumage traits may not be selectively equivalent.     

Population changes in Czech passerines are predicted by their life‐history and ecological traits

A species’ susceptibility to environmental change might be predicted by its ecological and life‐history traits. However, the effects of such traits on long‐term bird population trends have not yet been assessed using a comprehensive set of explanatory variables. Moreover, the extent to which phylogeny affects patterns in the interspecific variability of population changes is unclear. Our study focuses on the interspecific variability in long‐term population trends and annual population fluctuations of 68 passerine species in the Czech Republic, assessing the effects of eight life‐history and five ecological traits. Ordination of life‐history traits of 68 species revealed a life‐history gradient, from ‘r‐selected’ (e.g. small body mass, short lifespan, high fecundity, large clutch size) to ‘K‐selected’ species. r‐selected species had more negative population trends than K‐selected species, and seed‐eaters declined compared with insectivores. We suggest that the r‐selected species probably suffer from widespread environmental changes, and the seed‐eaters from current changes in agriculture and land use. Populations of residents fluctuated more than populations of short‐distance migrants, probably due to the effect of winter climatic variability. Variance partitioning at three taxonomic levels showed that whereas population trends, population fluctuations and habitat specialization expressed the highest variability at the species level, most life‐history traits were more variable at higher taxonomic levels. These results explain the loss of statistical power in the relationship between life histories and population trends after controlling for phylogeny. However, we argue that a lack of significance after controlling for phylogeny should not reduce the value of such results for conservation purposes.     

Positive correlations between pre‐ and post‐copulatory sexual traits in warblers

Theoretical models predict that investment in pre‐copulatory and post‐copulatory sexually selected traits should trade‐off. At the macroevolutionary scale, the majority of studies to date have focused on male weaponry as the target of pre‐copulatory sexual selection, but the trade‐off should equally apply to traits used to attract females, such as bird song and plumage. We studied the Old World leaf warblers (Phylloscopidae), a group of socially monogamous songbirds that experience relatively high levels of sperm competition. We examined the relationships between song duration and number of elements in the song with sperm length across 21 species, and between the same song variables and combined testes mass in a subset of these species (n = 10). Across species, these song variables and testes mass/sperm length were generally positively correlated, albeit not statistically significantly so or with borderline significance. In contrast to theory, we found no evidence for negative associations between pre‐ and post‐copulatory traits. We argue that this is a consequence of males of some species investing more into overall fertilization success (i.e. the sum of pre‐ and post‐copulatory sexual selection) than males of other species, and high fertilization success is achieved through investment into both mate attraction and sperm competition.     

The extent of variation in male song, wing and genital characters among allopatric Drosophila montana populations

Drosophila montana, a species of the Drosophila virilis group, has distributed around the northern hemisphere. Phylogeographic analyses of two North American and one Eurasian population of this species offer a good background for the studies on the extent of variation in phenotypic traits between populations as well as for tracing the selection pressures likely to play a role in character divergence. In the present paper, we studied variation in the male courtship song, wing and genital characters among flies from Colorado (USA), Vancouver (Canada) and Oulanka (Finland) populations. The phenotypic divergence among populations did not coincide with the extent of their genetic divergence, suggesting that the characters are not evolving neutrally. Divergence in phenotypic traits was especially high between the Colorado and Vancouver populations, which are closer to each other in terms of their mtDNA genotypes than they are to the Oulanka population. The males of the Colorado population showed high divergence especially in song traits and the males of the Vancouver population in wing characters. Among the male song traits, two characters known to be under sexual selection and a trait important in species recognition differed clearly between populations, implying a history of directional and/or diversifying rather than balancing selection. The population divergence in wing characters is likely to have been enhanced by natural selection associated with environmental factors, whereas the male genitalia traits may have been influenced by sexual selection and/or sexual conflict.     

The search for causal traits of speciation: Divergent female mate preferences target male courtship song,not pheromones,in Drosophila athabasca species complex

Understanding speciation requires the identification of traits that cause reproductive isolation. This remains a major challenge since it is difficult to determine which of the many divergent traits actually caused speciation. To overcome this difficulty, we studied the sexual cue traits and behaviors associated with rapid speciation between EA and WN sympatric behavioral races of Drosophila athabasca that diverged only 16,000–20,000 years ago. First, we found that sexual isolation was essentially complete and driven primarily by divergent female mating preferences. To determine the target of female mate choice, we found that, unlike cuticular hydrocarbons (CHCs), male courtship song is highly divergent between EA and WN in both allopatry and sympatry and is not affected by latitudinal variation. We then used pheromone rub‐off experiments to show no effect of CHCs on divergent female mate choice. In contrast, both male song differences and male mating success in hybrids exhibited a large X‐effect and playback song experiments confirmed that male courtship song is indeed the target of sexual isolation. These results show that a single secondary sexual trait is a major driver of speciation and suggest that we may be overestimating the number of traits involved in speciation when we study older taxa.     

Weak relationships of parasite infection with sexual and life‐history traits in wild‐caught Texas field crickets (Gryllus texensis)

1. Sex differences in immune investment and infection rate are predicted due to the divergent life histories of males and females, where females invest more toward immunity due to the fitness consequences of a reduced lifespan and males allocate less toward immunity due to increased resource investment in traits critical to sexual selection. Consequently, males are expected to fight infection less adeptly, resulting in higher parasite loads relative to females across all taxa.
2. Wild animals rarely face a single parasite within their given environment, yet nearly all studies on sex‐biased infection rates have focused on a single host–parasite relationship. Here, we investigate how simultaneous natural infections of ecto‐ and endosymbionts (i.e. both parasitic and phoretic taxa) correlate with sex biases in host immune response and reproductive investment in a field‐caught cricket, Gryllus texensis.
3. Our comprehensive analysis found no significant sex differences in two measures of immune response (melanization and nodulation), and found no strong evidence of a sex bias in the prevalence or intensity of parasitism by the three most common parasites infecting wild G. texensis field crickets (Eutrombidiidae, gregarines, and nematodes).
4. Two traits related to female fitness, egg number and egg size, showed no relation to parasitic infection; however, males having wider heads and poorer body condition were significantly more infected by eutrombidiid mites, gregarines, and nematodes.
5. Despite frequent predictions of male‐biased parasitism in the literature, our results concur with many other studies indicating that the divergent life histories of males and females alone are not sufficient to explain natural infection rates in wild insects.

     

Rarity in Chilean forest birds: which ecological and life‐history traits matter?

While it is a truism that species rarity is non-randomly distributed across regions, habitats, and taxa, there is little consensus on which factors are the best predictors of low abundances and restricted geographical ranges. In this study, we evaluate the effects of ecological and life-history traits, as well as phylogeny, on rarity in the abundance and distribution of land birds inhabiting forest habitats in the Mediterranean and temperate regions of Chile. We use data on abundance collected at 16 sites and data on latitudinal distribution obtained from a literature compilation. Statistical analyses were based on multiple regression and multivariate models. We used Signed Mantel test to analyse the relationship between species ecological and life-history traits and rarity, taking into account the effect of phylogenetic relatedness. We found that rarity, in terms of distribution, is associated with a low investment in reproduction, non-migratory status, and degree of habitat specialization. These ecological and life-history traits, in association with forest loss due to climatic changes and human impacts, may explain the narrow distribution of most endemic forest birds species. Rarity in abundance, on the other hand, is more difficult to explain. However, the fact that large species with an insectivorous diet showed low density in the assemblages studied suggests that abundance is mostly regulated by energy (resource) requirements and availability. Finally, our study shows that there is no phylogenetic influence in the observed patterns.     

Groupings of life‐history traits are associated with distribution of forest plant species in a fragmented landscape

Questions: 1. Do relationships among forest plant traits correspond to dispersability‐persistence trade‐offs or other inter‐trait correlations found in the literature? 2. Do species groups delineated by trait similarity, differ in occurrence in ancient vs. new forests or isolated vs more continuous forest patches? 3. Are these patterns consistent for different forest types? Location: Central Belgium, near Leuven. Methods: We investigate the distributions of a large set of plant traits and combinations among all forest species occurring in patches with varying forest continuity and isolation. Through calculation of Gower's similarity index and subsequent clustering,‘emergent’ species groups are delineated. Then, the relative occurrence of these different groups in forest patches of different age and size, sustaining different forest types (alluvial vs. Quercion), and having different isolation status is compared through multivariate GLM analysis. Results: Correlations among several life history traits point towards trade‐offs of dispersability and fecundity vs. longevity. We distinguished three species groups: 1= mainly shrubs or climbers with fleshy or wind dispersed fruits and high dispersal potential; 2 = dominated by small, mainly vegetatively reproducing herbs; 3 = with spring flowering herbs with large seeds and mainly unassisted dispersal. Relative occurrence of these groups was significantly affected by forest age, area, isolation and forest type. Separate analyses for alluvial and Quercion forests indicated that the relative importance of these factors may differ, depending on forest type and species group. Both forest continuity and isolation are important in restricting the relative occurrence of forest species in alluvial forests, whatever their group membership. In Quercion forests forest patch area was the primary determinant of relative occurrence of species groups. Conclusions: It is very important to preserve the actual forest area including the spatial setting and the dispersal infrastructure within the landscape. Next, forest connectivity may be restored, but it is inherently a long process.     

Variability in life‐history and ecological traits is a buffer against extinction in mammals

Anthropogenic degradation of the world's ecosystems is leading to a widespread and accelerating loss of biodiversity. However, not all species respond equally to existing threats, raising the question: what makes a species more vulnerable to extinction? We propose that higher intraspecific variability may reduce the risk of extinction, as different individuals and populations within a species may respond differently to occurring threats. Supporting this prediction, our results show that mammalian species with more variable adult body masses, litter sizes, sexual maturity ages and population densities are less vulnerable to extinction. Our findings reveal the role of local variation among populations, particularly of large mammals, as a buffering mechanism against extinction, and emphasise the importance of considering trait variation in comparative analyses and conservation management.     

Sex‐linked inheritance,genetic correlations and sexual dimorphism in three melanin‐based colour traits in the barn owl

Theory states that genes on the sex chromosomes have stronger effects on sexual dimorphism than genes on the autosomes. Although empirical data are not necessarily consistent with this theory, this situation may prevail because the relative role of sex‐linked and autosomally inherited genes on sexual dimorphism has rarely been evaluated. We estimated the quantitative genetics of three sexually dimorphic melanin‐based traits in the barn owl (Tyto alba), in which females are on average darker reddish pheomelanic and display more and larger black eumelanic feather spots than males. The plumage traits with higher sex‐linked inheritance showed lower heritability and genetic correlations, but contrary to prediction, these traits showed less pronounced sexual dimorphism. Strong offspring sexual dimorphism primarily resulted from daughters not expressing malelike melanin‐based traits and from sons expressing femalelike traits to similar degrees as their sisters. We conclude that in the barn owl, polymorphism at autosomal genes rather than at sex‐linked genes generate variation in sexual dimorphism in melanin‐based traits.     

Forest bees are replaced in agricultural and urban landscapes by native species with different phenologies and life‐history traits

Anthropogenic landscapes are associated with biodiversity loss and large shifts in species composition and traits. These changes predict the identities of winners and losers of future global change, and also reveal which environmental variables drive a taxon's response to land use change. We explored how the biodiversity of native bee species changes across forested, agricultural, and urban landscapes. We collected bee community data from 36 sites across a 75,000 km² region, and analyzed bee abundance, species richness, composition, and life‐history traits. Season‐long bee abundance and richness were not detectably different between natural and anthropogenic landscapes, but community phenologies differed strongly, with an early spring peak followed by decline in forests, and a more extended summer season in agricultural and urban habitats. Bee community composition differed significantly between all three land use types, as did phylogenetic composition. Anthropogenic land use had negative effects on the persistence of several life‐history strategies, including early spring flight season and brood parasitism, which may indicate adaptation to conditions in forest habitat. Overall, anthropogenic communities are not diminished subsets of contemporary natural communities. Rather, forest species do not persist in anthropogenic habitats, but are replaced by different native species and phylogenetic lineages preadapted to open habitats. Characterizing compositional and functional differences is crucial for understanding land use as a global change driver across large regional scales.     

Population structure,spatial distribution and life‐history traits of blacktip reef sharks Carcharhinus melanopterus

During a survey of the population of blacktip reef shark Carcharhinus melanopterus in Moorea (French Polynesia) between 2007 and 2011, population structural characteristics were estimated from 268 individuals. Total length (L_T) ranged from 48 to 139 cm and 48 to 157 cm for males and females, respectively, demonstrating that the average L_T of females was larger than that of males. The C. melanopterus population at Moorea showed an apparent spatial sexual segregation with females preferentially frequenting lagoons and males the fore‐reefs. Mean growth rate was c. 6 cm year^?1. Males reached sexual maturity at 111 cm L_T. This study reports on the population characteristics of this widespread carcharhinid shark species and makes comparisons with other locations, confirming high geographic variability in the population structure of the species.     

Cross‐generational effects of temperature on flight performance,and associated life‐history traits in an insect

Nongenetic parental effects may affect offspring phenotype, and in species with multiple generations per year, these effects may cause life‐history traits to vary over the season. We investigated the effects of parental, offspring developmental and offspring adult temperatures on a suite of life‐history traits in the globally invasive agricultural pest Grapholita molesta. A low parental temperature resulted in female offspring that developed faster at low developmental temperature compared with females whose parents were reared at high temperature. Furthermore, females whose parents were reared at low temperature were heavier and more fecund and had better flight abilities than females whose parents were reared at high temperature. In addition to these cross‐generational effects, females developed at low temperature had similar flight abilities at low and high ambient temperatures, whereas females developed at high temperature had poorer flight abilities at low than at high ambient temperature. Our findings demonstrate a pronounced benefit of low parental temperature on offspring performance, as well as between‐ and within‐generation effects of acclimation to low temperature. In cooler environments, the offspring generation is expected to develop more rapidly than the parental generation and to comprise more fecund and more dispersive females. By producing phenotypes that are adaptive to the conditions inducing them as well as heritable, cross‐generational plasticity can influence the evolutionary trajectory of populations. The potential for short‐term acclimation to low temperature may allow expanding insect populations to better cope with novel environments and may help to explain the spread and establishment of invasive species.