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

2020 ◽  
Author(s):  
William Toubiana ◽  
David Armisén ◽  
Corentin Dechaud ◽  
Roberto Arbore ◽  
Abderrahman Khila

AbstractExaggerated 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 sex-specific phenotypes, and how these changes are reflected in genomic architecture. This is primarily due to the lack of a representative genome and transcriptomes to study the development of secondary sexual 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 used as weapons. The quality of the genome assembly is such that over 90% of the sequence is captured in 13 scaffolds. The most exaggerated legs in males were particularly enriched in sex-biased genes, indicating a specific signature of gene expression in association with sex-specific 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. Interestingly, we found that female-biased genes that are expressed in the third legs only, but not male-biased genes, were over-represented in the X chromosome compared to the autosomes. An enrichment analysis for sex-biased genes along the chromosomes revealed that they can 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. Our findings shed light on how directional sexual selection drives sex-biased gene expression and genome architecture along the path to trait exaggeration and sexual dimorphism.

BMC Biology ◽  
2021 ◽  
Vol 19 (1) ◽  
Author(s):  
William Toubiana ◽  
David Armisén ◽  
Corentin Dechaud ◽  
Roberto Arbore ◽  
Abderrahman Khila

Abstract 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.


2015 ◽  
Vol 93 (5) ◽  
pp. 397-402
Author(s):  
M.A. Owen ◽  
D.C. Lahti

Secondary sexual traits tend to be sexually dimorphic, and theory predicts that such traits should also be condition-dependent in a sex-specific manner. We investigate these phenomena in a field study of the small Indian mongoose (Herpestes auropunctatus (Hodgson, 1836); formerly Herpestes javanicus (É. Geoffroy Saint-Hillaire, 1818)), in the first attempt at understanding secondary sexual traits and sexual selection in this species. Small Indian mongooses are solitary and nonterritorial, and they likely depend on chemical (scent) rather than visual or acoustic signals for communication. Additionally, they possess a fleshy projection around their anus, the anal pad, thought to aid in scent-marking. Our results revealed strong male-biased sexual dimorphism in mass, skull and body lengths, canine diameters, and anal pad area. After controlling for the influence of body length, males were 31% heavier and possessed anal pads that were 68% larger than females’. Additionally, anal pad size was positively related to body size in males but not in females and was condition-dependent in males but not in females. Taken together, our findings provide indirect evidence that the anal pad might have evolved, at least in part, via sexual selection.


2021 ◽  
Vol 288 (1950) ◽  
Author(s):  
Wendy A. Valencia-Montoya ◽  
Tiago B. Quental ◽  
João Filipe R. Tonini ◽  
Gerard Talavera ◽  
James D. Crall ◽  
...  

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.


2000 ◽  
Vol 78 (7) ◽  
pp. 1199-1206 ◽  
Author(s):  
Claudia Palestrini ◽  
Antonio Rolando ◽  
Paola Laiolo

Allometric relationships in primary sexual traits (male and female genitalia), secondary sexual traits (male horns and female carinae), and non-sex-related traits (external body traits, epipharynx traits) were studied in the dung beetle Onthophagus taurus. Model II regressions of log-transformed data were used to quantify relationships, with pronotum width as regressor and indicator of overall body size. Slopes (allometric values) for the different trait categories were significantly different, with secondary sexual traits showing the highest values (higher than 1.0), followed by external body traits (slightly lower than 1.00) and epipharynx traits (around 0.2). Primary sexual traits and body size were mostly uncorrelated and genital sizes were virtually constant. Allometries of secondary sexual traits were quite different in the two sexes: the relationship between male horn length and pronotum width was approximately sigmoidal, while that between female carina length and pronotum width was linear. External body traits had significantly higher allometric values in females than in males. Our results suggest that traits in the different categories are under different kinds of selection. Genital allometries can be explained on the basis of sexual selection by cryptic female choice or by the lock-and-key hypothesis. Among secondary sexual characters, male horn morphology seems to be mostly "environmentally" determined and sexual selection would affect only a component of the developmental mechanism of horn expression. External body characters are likely under natural selection, even though a few traits could be sex-related. Finally, in both sexes, internal epipharynx traits seem to be subject to the same selective pressure, probably because males and females use the same feeding niche. The constancy of genital sizes in O. taurus suggests that in developmental processes, more is invested in primary sexual traits (to produce genitalia of the proper size) than in secondary sexual or body traits. Males receiving low quantities of food may incur costs associated with a small horn or small body size, but do not incur costs associated with small genitalia. Females probably share the same developmental pattern.


2013 ◽  
Vol 26 (4) ◽  
pp. 912-918 ◽  
Author(s):  
Rhonda R. Snook ◽  
Nelly A. Gidaszewski ◽  
Tracey Chapman ◽  
Leigh W. Simmons

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