Hox genes mediate the escalation of sexually antagonistic traits in water striders

Crumière, Antonin Jean Johan; Khila, Abderrahman

doi:10.1098/rsbl.2018.0720

Cited by 12 publications

(10 citation statements)

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“…sp. is the only species in this sample where males’ third legs possess a prominent set of spines that are not found in the females, indicative of sexually antagonistic selection [ 32 , 33 ] ( Fig 3I ). Surprisingly, BMP11 RNAi reduced or removed these spines ( Fig 3J ), indicating that this gene could also play a role in the development of discrete sexually dimorphic traits.…”

Section: Resultsmentioning

confidence: 99%

The growth factor BMP11 is required for the development and evolution of a male exaggerated weapon and its associated fighting behavior in a water strider

et al. 2021

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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 among individuals of the same population. While the evolution of allometry has attracted much attention for centuries, our understanding of the developmental genetic mechanisms underlying its emergence remains fragmented. Here we conduct comparative transcriptomics of the legs followed by an RNA interference (RNAi) screen to identify genes that play a role in the hyperallometric growth of the third legs in the males of the water strider Microvelia longipes. 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 slope and mean body size in males. In contrast, BMP11 RNAi reduced mean body size but did not affect slope either in the females of M. longipes or in the males and females of other closely related Microvelia species. 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. Therefore, male body size, the exaggerated weapon, and the intense fighting behavior associated with it are genetically correlated in M. longipes. Our results support a possible role of pleiotropy in the evolution of allometric slope.

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Section: Resultsmentioning

confidence: 99%

The growth factor BMP11 is required for the development and evolution of a male exaggerated weapon and its associated fighting behavior in a water strider

et al. 2021

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“…Comparing the three pairs of legs in M. longipes offers a unique opportunity to understand how gene regulation correlates with phenotypic differences between males and females, as these legs present different types and degrees of sexual dimorphism, including discrete and quantitative phenotypes [ 40 , 41 ]. For example, the development of the sex-comb, a discrete phenotype known to be under stabilizing selection [ 63 , 64 ], occurs in the first legs of males during the 5th instar [ 65 ]. In contrast, the exaggerated growth of male third legs, a quantitative trait which also occurs during the 5th nymphal instar [ 40 ], is an example of directional sexual selection that is absent, or at least reduced, in the two other male legs and in females legs [ 41 ].…”

Section: Discussionmentioning

confidence: 99%

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

et al. 2021

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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.

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“…There are ample opportunities among aquatic insects, as they have been estimated to comprise about 6% of all insect diversity, with likely more than 200,000 species 32 . Furthermore, RNAi has already been performed on water striders that tend to inhabit the surface of aquatic environments 33 . If no genome is present, then a transcriptome can be assembled de novo.…”

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RNA Interference in Aquatic Beetles as a Powerful Tool for Manipulating Gene Expression at Specific Developmental Time Points

Rathore

Hassert

Clark-Hachtel

et al. 2020

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RNA interference (RNAi) remains a powerful technique that allows for the targeted reduction of gene expression through mRNA degradation. This technique is applicable to a wide variety of organisms and is highly efficient in the species-rich order Coleoptera (beetles). Here, we summarize the necessary steps for developing this technique in a novel organism and illustrate its application to the different developmental stages of the aquatic diving beetle Thermonectus marmoratus. Target gene sequences can be obtained cost-effectively through the assembly of transcriptomes against a close relative with known genomics or de novo. Candidate gene cloning utilizes a specific cloning vector (the pCR4-TOPO plasmid), which allows the synthesis of double-stranded RNA (dsRNA) for any gene with the use of a single common primer. The synthesized dsRNA can be injected into either embryos for early developmental processes or larvae for later developmental processes. We then illustrate how RNAi can be injected into aquatic larvae using immobilization in agarose. To demonstrate the technique, we provide several examples of RNAi experiments, generating specific knockdowns with predicted phenotypes. Specifically, RNAi for the tanning gene laccase2 leads to cuticle lightening in both larvae and adults, and RNAi for the eye pigmentation gene white produces a lightening/lack of pigmentation in eye tubes. In addition, the knockdown of a key lens protein leads to larvae with optical deficiencies and a reduced ability to hunt prey. Combined, these results exemplify the power of RNAi as a tool for investigating both morphological patterning and behavioral traits in organisms with only transcriptomic databases. 11.

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Hox genes mediate the escalation of sexually antagonistic traits in water striders

Cited by 12 publications

References 35 publications

The growth factor BMP11 is required for the development and evolution of a male exaggerated weapon and its associated fighting behavior in a water strider

The growth factor BMP11 is required for the development and evolution of a male exaggerated weapon and its associated fighting behavior in a water strider

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

RNA Interference in Aquatic Beetles as a Powerful Tool for Manipulating Gene Expression at Specific Developmental Time Points

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