Relationships between male secondary sexual traits, physiological state and offspring viability in the three-spined stickleback

Background Sexual signals produced by males play a central role in sexual selection, but the relationship between these traits and the quality of the bearer are often ambiguous. Secondary sexual traits may represent genetic quality of the bearer, resulting in positive relationships with physiological state, or may be costly to produce, showing trade-off with physiological state. A number of studies have explored the relationships between secondary sexual traits and other functional traits, but few have studied their fitness consequences. We studied the link between diverse physiological traits and both morphological and behavioural sexual traits and examined how their interplay influences offspring viability in the three-spined stickleback. Results Male sticklebacks showing nest building and courtship behaviour were smaller than those not investing in reproductive activities. There was no evidence that the expression of red nuptial colouration and the quality of courtship behaviour of males are positively related to their metabolic rates, swim ability, oxidative damage and mtDNA copy number. However, individuals showing larger red nuptial colour areas had higher levels of oxidative DNA damage in their sperm. Male courtship behaviour and aggressiveness, but not red colour area, were good predictors of offspring hatching and survival. Conclusions Our results suggest that, in our study population at the southern edge of the species’ distribution, sexual colouration of male sticklebacks was not a good indicator of their body state, but both courtship quality and aggressiveness during the courtship are reliable cues of their gamete quality, influencing the viability of their offspring. Thus, females that choose mates based on their courtship behaviour will have high fitness. In the study population, which represents a fast pace-of-life with high reproductive rate and short lifespan, sexual ornaments of males may not honestly signal their physiological and physical state because they invest at maximum in a single reproductive season despite high costs.

Sex Reversal and Performance in Fitness-Related Traits During Early Life in Agile Frogs

Sex reversal is a mismatch between genetic sex (sex chromosomes) and phenotypic sex (reproductive organs and secondary sexual traits). It can be induced in various ectothermic vertebrates by environmental perturbations, such as extreme temperatures or chemical pollution, experienced during embryonic or larval development. Theoretical studies and recent empirical evidence suggest that sex reversal may be widespread in nature and may impact individual fitness and population dynamics. So far, however, little is known about the performance of sex-reversed individuals in fitness-related traits compared to conspecifics whose phenotypic sex is concordant with their genetic sex. Using a novel molecular marker set for diagnosing genetic sex in agile frogs (Rana dalmatina), we investigated fitness-related traits in larvae and juveniles that underwent spontaneous female-to-male sex reversal in the laboratory. We found only a few differences in early life growth, development, and larval behavior between sex-reversed and sex-concordant individuals, and altogether these differences did not clearly support either higher or lower fitness prospects for sex-reversed individuals. Putting these results together with earlier findings suggesting that sex reversal triggered by heat stress may be associated with low fitness in agile frogs, we propose the hypothesis that the fitness consequences of sex reversal may depend on its etiology.

Evidence of Sex Differentiation Based on Morphological Traits During the Early Development Stage of Mud Crab Scylla paramamosain

In order to uncover the sexual difference in morphology and how early they appear during the development stage of mud crab Scylla paramamosain, we measured, observed, and biostatistically analyzed morphological traits related to sex. For unveiling the morphological differences between sexes, morphological traits involving abdomen width (AW), carapace length (CL), and carapace width (CW) were first measured during the crablet development stage of S. paramamosain in the present study. The correlation analyses and path analyses exhibited that sexual dimorphism in the third abdomen width (AW3) and fourth abdomen width (AW4) could be used for sex identification from stage C VI (stage VI of crablet). Based on the stepwise discriminant analysis and standardized traits, a sex discriminant equation was constructed, which is capable for sex identification in crablets from stage C VI. Observations for secondary sexual traits and abdomen morphology (shape and pleopods) using a dissecting microscope or scanning electron microscope indicated that sexes are easily identified at stage C VIII according to the abdomen shape; meanwhile, at stage C II based on pleopod difference, and at stage C I by the presence or absence of gonopores. The findings in this study contribute greatly to the accuracy of sex identification of S. paramamosain during the early development stage, which promotes the understanding of the morphological differentiation mechanism of sex.

Allometry, sexual selection, and evolutionary lines of least resistance shaped the evolution of exaggerated sexual traits within the genus Tyrannus

Variational properties hold a fundamental role in shaping biological evolution, exerting control over the magnitude and direction of evolutionary change elicited by microevolutionary processes that sort variation, such as selection or drift. We studied the Tyrannus genus, as a model for examining the conditions and drivers that facilitate the repeated evolution of exaggerated, secondary sexual traits in the face of significant functional limitations. We study the role of allometry, sexual selection, and their interaction on the diversification of tail morphology in the genus, assessing whether and how they promoted or constrained phenotypic evolution. The exaggerated and functionally-constrained long feathers of deep-forked species, T. savana and T. forficatus, independently diverged from the rest of the genus following the same direction of main interspecific variation common to the entire cluster of species. However, at a macroevolutionary scale those axes summarising both sexual dimorphism and allometric variation of the deep-forked species were aligned with the between-species maximum variation axis of non deep-forked species. Thus, we are presenting evidence of amplified divergence via the co-option and reorientation of allometric shape variation involved in a sexual selection process that repeatedly drove morphology along a historically favoured direction of cladogenetic evolution.

Facultative release from developmental constraints through polyphenism promotes adaptively flexible maturation

The timing of maturation, a critical fitness determinant, is influenced by developmental and energetic constraints, particularly when growth is poor in adverse conditions. Such constraints can be altered through developmental plasticity. Thus, in theory, plasticity in energetically costly sexually selected morphologies can promote life history flexibility in variable environments. We experimentally tested this hypothesis in bulb mites (Rhizoglyphus robini) that polyphenically develop as armed fighters with enlarged legs or as scramblers without modified legs. We found that (i) mites enter metamorphosis earlier if they develop as scramblers, (ii) mites accelerate the onset of metamorphosis when they sense resource limitation, and (iii) scrambler expression increases under increased competition for food, enabling males to mature early and escape juvenile mortality. We propose that life history plasticity can evolve through polyphenic release from sexually selected constraints, making the evolutionary dynamics of secondary sexual traits and life history traits, typically studied separately, interdependent.

Nutrient-dependent allometric plasticity in a male-diphenic mite

Male secondary sexual traits often scale allometrically with body size. These allometries can be variable within species, and may shift depending on environmental conditions such as food quality. Such allometric plasticity has been hypothesized to initiate local adaptation and evolutionary diversification of scaling relationships, but is under-recorded, and its eco-evolutionary effects are not well understood. Here, we test for allometric plasticity in the bulb mite (Rhizoglyphus robini) in which large males tend to develop as armed adult fighters with thickened third legs, while small males become adult scramblers without thickened legs. We first examined the ontogenetic timing for size- and growth-dependent male morph determination, using experimentally amplified fluctuations in growth rate throughout juvenile development. Having established that somatic growth and body size determine male morph expression immediately before metamorphosis, we examined whether the relationship between adult male morph and size at metamorphosis shifts with food quality. We found that the threshold body size for male morph expression shifts towards lower values with deteriorating food quality, confirming food-dependent allometric plasticity. Such allometric plasticity may allow populations to track prevailing nutritional conditions, potentially facilitating rapid evolution of allometric scaling relationships.

Evolutionary trade-offs between male secondary sexual traits revealed by a phylogeny of the hyperdiverse tribe Eumaeini (Lepidoptera: Lycaenidae)

Male butterflies in the hyperdiverse tribe Eumaeini possess an unusually complex and diverse repertoire of secondary sexual characteristics involved in pheromone production and dissemination. Maintaining multiple sexually selected traits is likely to be metabolically costly, potentially resulting in trade-offs in the evolution of male signals. However, a phylogenetic framework to test hypotheses regarding the evolution and maintenance of male sexual traits in Eumaeini has been lacking. Here, we infer a comprehensive, time-calibrated phylogeny from 379 loci for 187 species representing 91% of the 87 described genera. Eumaeini is a monophyletic group that originated in the late Oligocene and underwent rapid radiation in the Neotropics. We examined specimens of 818 of the 1096 described species (75%) and found that secondary sexual traits are present in males of 91% of the surveyed species. Scent pads and scent patches on the wings and brush organs associated with the genitalia were probably present in the common ancestor of Eumaeini and are widespread throughout the tribe. Brush organs and scent pads are negatively correlated across the phylogeny, exhibiting a trade-off in which lineages with brush organs are unlikely to regain scent pads and vice versa . In contrast, scent patches seem to facilitate the evolution of scent pads, although they are readily lost once scent pads have evolved. Our results illustrate the complex interplay between natural and sexual selection in the origin and maintenance of multiple male secondary sexual characteristics and highlight the potential role of sexual selection spurring diversification in this lineage.

Impact of male trait exaggeration on sex-biased gene expression and genome architecture in a water strider

Background Exaggerated secondary sexual traits are widespread in nature and often evolve under strong directional sexual selection. Although heavily studied from both theoretical and empirical viewpoints, we have little understanding of how sexual selection influences sex-biased gene regulation during the development of exaggerated secondary sexual phenotypes, and how these changes are reflected in genomic architecture. This is primarily due to the limited availability of representative genomes and associated tissue and sex transcriptomes to study the development of these traits. Here we present the genome and developmental transcriptomes, focused on the legs, of the water strider Microvelia longipes, a species where males exhibit strikingly long third legs compared to females, which they use as weapons. Results We generated a high-quality genome assembly with 90% of the sequence captured in 13 scaffolds. The most exaggerated legs in males were particularly enriched in both sex-biased and leg-biased genes, indicating a specific signature of gene expression in association with trait exaggeration. We also found that male-biased genes showed patterns of fast evolution compared to non-biased and female-biased genes, indicative of directional or relaxed purifying selection. By contrast to male-biased genes, female-biased genes that are expressed in the third legs, but not the other legs, are over-represented in the X chromosome compared to the autosomes. An enrichment analysis for sex-biased genes along the chromosomes revealed also that they arrange in large genomic regions or in small clusters of two to four consecutive genes. The number and expression of these enriched regions were often associated with the exaggerated legs of males, suggesting a pattern of common regulation through genomic proximity in association with trait exaggeration. Conclusion Our findings indicate how directional sexual selection may drive sex-biased gene expression and genome architecture along the path to trait exaggeration and sexual dimorphism.