Sexual dimorphism and heightened conditional expression in a sexually selected weapon in the Asian rhinoceros beetle

Zinna, Robert A.; Emlen, Douglas J.; Lavine, Laura Corley; Johns, Annika; Gotoh, Hiroki; Niimi, Teruyuki; Dworkin, Ian

doi:10.1111/mec.14907

Cited by 37 publications

(43 citation statements)

References 116 publications

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“…We identified a signature of leg exaggeration among sex-biased genes. Consistent with studies of sex-biased gene expression 5,44–46 , we found that the degree of sexual dimorphism is associated with different patterns of expression among these genes (Figure 2&3). In our dataset, the most exaggerated legs mobilized more differentially expressed genes between the sexes and a higher degree of differential expression, especially in male-biased genes.…”

Section: Discussionsupporting

confidence: 90%

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

Toubiana¹,

Armisén²,

Dechaud³

et al. 2020

Preprint

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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 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.

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Section: Discussionsupporting

confidence: 90%

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

Toubiana¹,

Armisén²,

Dechaud³

et al. 2020

Preprint

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show abstract

“…Since gene expression was measured from whole animal bodies, interpretation of results is however potentially complicated by differential allometric scaling of tissues in males and females in different condition [18,19]. Sex-biased gene expression in response to environmental quality has also been studied for various tissues in developing scarab beetles [20][21][22]. Results from these studies also show that the number of sex-biased genes covary positively with environmental quality in general, but not for all tissues tested.…”

Section: Introductionmentioning

confidence: 99%

Heightened condition-dependence of the sexual transcriptome as a function of genetic quality in Drosophila melanogaster head tissue

et al. 2019

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Theory suggests sexual traits should show heightened condition-dependent expression. This prediction has been tested extensively in experiments where condition has been manipulated through environmental quality. Condition-dependence as a function of genetic quality has, however, only rarely been addressed, despite its central importance in evolutionary theory. To address the effect of genetic quality on expression of sexual and non-sexual traits, we here compare gene expression in Drosophila melanogaster head tissue between flies with intact genomes (high condition) and flies carrying a major deleterious mutation (low condition). We find that sex-biased genes show heightened condition-dependent expression in both sexes, and that expression in low condition males and females regresses towards a more similar expression profile. As predicted, sex-biased expression was more sensitive to condition in males compared to females, but surprisingly female-biased, rather than male-biased, genes show higher sensitivity to condition in both sexes. Our results thus support the fundamental predictions of the theory of condition-dependence when condition is a function of genetic quality.

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“…Exaggerated traits represent striking cases of differential growth between various organs, and we are just beginning to understand the underlying developmental genetic processes 5,30 . Studies in various insects suggest that traits would achieve exaggeration via their increased sensitivity to systemic growth factors such as Juvenile Hormone or Insulin 7,10,11,31,32 .…”

Section: Discussionmentioning

confidence: 99%

Pleiotropy promotes male exaggerated weapon and its associated fighting behaviour in a water strider

Toubiana¹,

Armisén²,

Decaras³

et al. 2020

Preprint

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Exaggerated sexually selected traits, often carried by males, are characterized by the evolution of hyperallometry, resulting in their disproportionate growth relative to the rest of the body 1–3. While the evolution of allometry has attracted much attention for centuries, our understanding of the developmental genetic mechanisms underlying its emergence remains fragmented 4,5. Here we show that the hyperallometric legs in the males of the water strider Microvelia longipes are associated with a specific signature of gene expression during development. Using RNAi knockdown, we demonstrate that a broadly expressed growth factor, Bone Morphogenetic Protein 11 (BMP11, also known as Growth Differentiation Factor 11), regulates leg allometries through increasing the allometric coefficient and mean body size in males. In contrast, BMP11 RNAi reduced mean body size but did not affect slope in females. Furthermore, our data show that a tissue specific factor, Ultrabithorax (Ubx), increases intercept without affecting mean body size. This indicates a genetic correlation between mean body size and variation in allometric slope, but not intercept. Strikingly, males treated with BMP11 RNAi exhibited a severe reduction in fighting frequency compared to both controls and Ubx RNAi-treated males. Overall, we demonstrate a genetic correlation between male body size, the exaggerated weapon, and the intense fighting behaviour associated with it in M. longipes. Our results provide evidence for a role of pleiotropy in the evolution of allometric slope.

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Sexual dimorphism and heightened conditional expression in a sexually selected weapon in the Asian rhinoceros beetle

Cited by 37 publications

References 116 publications

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

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

Heightened condition-dependence of the sexual transcriptome as a function of genetic quality in Drosophila melanogaster head tissue

Pleiotropy promotes male exaggerated weapon and its associated fighting behaviour in a water strider

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