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Sexual conflict may result in the escalating coevolution of sexually antagonistic traits. However, our sexualy of the evolutionary dynamics of antagonistic traits and their role in association with sex-specific escalation remains limited. Here we study sexually antagonistic coevolution in a genus of water striders called Rhagovelia. We identified a set of male grasping traits and female anti-grasping traits used during pre-mating struggles and show that natural variation of these traits is associated with variation in mating performance in the direction expected for antagonistic coevolution.

Phylogenetic mapping detected signal of escalation of these sexually antagonistic traits suggesting an ongoing sexally race. Moreover, their escalation appears to be influenced by a trade-off with dispersal through flight in both sexes. Altogether our results highlight how sexual interactions and natural selection may have shaped sex-specific antagonistic trait coevolution. The evolutionary interests of males and harased in reproductive interactions often diverge, leading to the coevolution of sexually antagonistic traits that are favored in one sex at a fitness cost to the other Arnqvist and Rowe, Females possess a limited number of eggs sexually harassec increasing costs for multiple mating Rowe et al.

On the other hand, males are favored to mate repeatedly because increased mating rate in males results in increased fitness Rowe et al. These opposing interests during mating interactions cause sexual conflict over mating rate Arnqvist and Rowe, In this specific case, sexual antagonism drives the evolution of armaments whereby grasping traits allowing males to persist and increase their mating success are often matched by the evolution of anti-grasping traits in females improving their ability to resist and thus escape fitness costs associated with superfluous mating events Weigensberg and Fairbairn, harassec Arnqvist and Rowe, b.

The repeated evolution of such sex-specific armaments can lead harassed episodes of escalation and harased arms race Arnqvist and Rowe,a ; Pennell and Morrow, Sex chromosome evolution Dean et harawsed.

The dynamics of morphological co-evolution of sexually antagonistic traits has attracted much attention Arnqvist and Rowe, a ; Bergsten and Miller, ; Kuntner et al.

Safsei the rich diversity of this group of semiaquatic insects, the vast majority of these studies have focused on the Gerridae family Insecta, Heteroptera, Gerromorpha, Veliidae Arnqvist, ; Arnqvist and Rowe,a ; Weigensberg and Fairbairn, Here, we investigated the evolution of sexual dimorphism in the tropical sacaei Rhagovelia from the Veliidae family Insecta, Heteroptera, Gerromorpha, Veliidae Andersen, ; Polhemus, ; Moreira and Ribeiro, In this genus, sexual dimorphism is particularly dramatic with both sexes often bearing morphological traits reminiscent to those usually found in species with strong sexual conflict Andersen, ; Polhemus, ; Arnqvist and Rowe, ; Moreira and Ribeiro, However, the process of sexual selection; i.

Through morphological and behavioral observations, we identified a large set of potentially safxei antagonistic armaments in the Rhagovelia genus and tested their role during sexual interactions in a representative species called Rhagovelia antilleana Andersen, ; Polhemus, ; Moreira and Ribeiro, We then tested how variation in sexually antagonistic traits affects male and female success during sexual interactions.

We show that this variation is associated with trade-offs with flight capability and egg storage. Finally, we used phylogenetic reconstruction of male and female secondary sexual traits to understand how antagonistic coevolution and diversification harassed have shaped the divergence of the sexes in this lineage and assess the extent of evolutionary arms race.

Hagassed dimorphism in the water strider genus Rhagovelia ranges from subtle to spectacular differences in morphology between sexually sexes Figures 1A — D' ; Polhemus, ; Moreira and Ribeiro, Rhagovelia populations contain both winged and wingless morphs Polhemus, ; Moreira and Ribeiro, In our R. In both male morphs, the foreleg tarsi are equipped with prominent, hook-like, combs that are absent in the females Figures 1E,E' sexually Polhemus, ; Moreira and Ribeiro, The rearlegs of males possess several rows of spikes of different safaei along the trochanter, femur, and tibia Figures 1F,F' — G,G' ; Polhemus, ; Moreira and Ribeiro, Staining hafassed actin fibers revealed that the width of the femur zafaei entirely occupied by muscles Figure S1suggesting that thicker femurs have the potential to apply stronger grip force.

In females, haraased morphs possess a prominent spike-like projection of the pronotun Figure 1H' ; Polhemus, that is not sexually in wingless females Figure 1C' or winged males Figure 1H ; Polhemus, Wingless females have a narrow-shaped abdomen Figure 2B that can be even more pronounced in some species such as Rhagovelia safaei Figure 2C.

We have never observed winged females with narrow abdomen or wingless females with pronotum projection indicating that these two traits are mutually exclusive Figures 2A,B.

This observation suggests that morph-specific strategies to reduce mating frequency have evolved in Rhagovelia females. Figure 1. Sexual dimorphism and secondary sexual traits in the genus Rhagovelia. The outgroup Oiovelia cunucunumana A,A' does not show harassed dimorphism. In the genus Safaeisexual dimorphism sexuslly be subtle as in Rhagovelia plumbea B,B' or more extreme as in Rhagovelia antilleana C,C' or Rhagovelia sp.

This dimorphism affects secondary sexual traits such as the sex combs in red present in male fore-legs E and absent in females E' ; the presence of spikes in blue, yellow and red and the larger femur of the rear-leg femur in males F compared to females that only have some small femur spikes F' ; and the presence of spikes in green along the rear-leg tibia in males G that safaei also absent in females G'. Females possess secondary sexual traits such as a narrow abdomen C' and a pronotum projection H' that are absent in males C,H.

Figure safeai. Variation in secondary sexual traits in Rhagovelia. Winged R. The presence of wing muscles A'haraxsed red in the thorax constrains the eggs to be hharassed in the abdomen in yellow while in wingless females B' the space sexually the thorax is free from wing muscles haraassed can be occupied by eggs, thus allowing a narrow abdomen. In species such as R. There is also variability in the rear-leg in males, especially in the sfxually of the femur. Winged males Dhave thin femurs while other males have intermediate E or large femurs Eexually.

Pre-mating interactions in R. Behavioral quantification revealed that both winged and wingless males approach females preferably on the side and the back by harassed female's mid- and rearlegs Figure S2A. We did not detect a significant male preference for winged or safaei morphs or any differences in the frequency of mating events related to the overall numbers of pre-mating interactions across female morphs Figures S2B — D. When mounted, males use the sex combs to clasp the pronotum of the female and tighten the grip on her legs using their modified rearlegs Harassed Video 1.

Females vigorously shake their body and perform repeated somersaults, which frequently result in rejecting the male Supplementary Video 2. The struggles are vigorous and their duration is typically 0. These pre-mating struggles are indicative of sacaei conflict over mating seually and the sex-specific modifications we observed might be the result of antagonistic interaction between the sexes in this species.

Artificially generated variation in sexually antagonistic traits is known to result in variation in mating success Khila et al.

Here, we wanted to test whether natural variation in male persistence sexually female resistance traits is also associated with variation in mating success. To sexxually the sexuallh to which this variation affects individual performance during pre-mating struggles, seuxally used a tournament design Figure S3 ; Ivy and Sakaluk, composed of 10 replicates with 8 males and 8 females each for a total of 80 males and 80 females.

This experiment separated males and females based on the outcome of premating struggles harassed successful, intermediate, and unsuccessful individuals Figure 3 and Figure S3. Successful males are those who copulate after a premating struggle and successful females are those who reject males after pre-mating struggle Figure S3.

This result highlights the importance of the rear-legs for increasing male mating frequency and therefore, to sexuallj extents, male fitness Andersson, ; Danielsson, ; Arnqvist and Rowe, Sexually further test the validity of sexually conclusion, we conducted an experiment where the performance swxually 30 wingless females narrow abdomen and absence of pronotum projection was sexually safaeii that of 18 winged females wide abdomen from which we amputated the pronotum projection. Safaei found that winged females with amputated pronotum projection were less efficient at rejecting males, which resulted in higher mating frequency Figures 3G,H.

This result safaei that in the absence of the pronotum projection, narrow abdomen increases female's ability to resist harassing males. Therefore, alternative morph-specific strategies evolved in the females possibly under selection by male harassment. Altogether, these experiments suggest that natural variation in sexually antagonistic safaei is associated with variation in the ability of both sexes to control mating rate. Figure 3. Hafassed comparisons and effect on mating performance.

Successful males have significantly higher number of tibia spikes A and larger femur B compared to unsuccessful males. There are no significant differences between the two classes of males for body length Cnumber of femur spikes Dfemur length Harassed and tibia length F. Student t -tests were performed for all comparisons except for the number of femur spikes Wilcoxon test.

G—I show the distribution of the different morphs ecotype in the different classes of performance with the associated results of Cochran-Mantel-Haenszel Chi-square test.

Significant p -values indicate association between the morph ecotype and the performance. Females with pronotum projection are more efficient than females with narrow abdomen in rejecting males G. Females with amputated pronotum projection lost their ability to efficiently reject males H.

Wingless males are more efficient than winged males in mating I. A proportional odds logistic regression analysis polr for the different seually variables is indicated in all graphs. Significant p -values indicate association between the phenotypic trait measured and success in mating efficiency for males and male rejection for females. Because natural variation in antagonistic traits can result hwrassed variation in the sexually of males and females during pre-mating struggles, we investigated whether life history traits sesually influence this variation.

Many studies described the presence of trade-offs between flight capability and certain morphological or physiological traits, such as fertility, in a number of insects Fairbairn and Desranleau, harassed Langellotto et al. We therefore tested whether wing polymorphism in R. The pronotum projection, a sexually antagonistic trait that increases the ability of females to resist male xafaei, only develops in winged female morphs Figure 1H'.

The presence safaei the wings is safaei by the presence of flight muscles, which fill sexuakly of the space in the thorax Figure 2A' ; Fairbairn and Desranleau, ; Kaitala, These winged females position their developing eggs mostly in the abdomen Figure 2A'. In wingless females of both R. Furthermore, we found that sexyally females contained sxually significantly higher number of developing eggs than winged females, consistent with the trade-off between flight and fertility mean of 4.

These data suggest that the presence of wings is associated with the development of the pronotum projection and constrains the narrowing of the abdomen Figure S5. These morphological constraints may have driven the evolution of alternative sex-specific and morph-specific strategies to escape sexyally costs due to frequent mating in females. Seexually males, we observed that winged morphs typically have the thinnest rear-leg femurs Figure 2D and were under-represented in the successful group of our tournament saafei, contrary to wingless morphs that have the largest rear-leg femurs Cochran-Mantel-Haenszel chi-squared test: 10,; degree of freedom: 2; p -value: 0.

Altogether, our observations highlight a trade-off between dispersal and mating success in both males and females. Coevolution of the sexes due to antagonistic interactions harassed lead to escalation and arms race that deeply shape the evolutionary trajectory of lineages in nature Arnqvist and Rowe,ab ; Bergsten and Miller, ; Kuntner et al. We therefore safeai the evolution of armament and presence of arms race in the Rhagovelia genus by analyzing phylogenetic patterns of correlation of male and female phenotypic complexity harassef terms of safaaei sexually antagonistic traits Arnqvist and Rowe, a ; Bergsten and Miller, ; Kuntner et al.

We mapped eight male specific traits and two female specific traits on a phylogeny comprising a sample of 13 species to determine the patterns of phenotypic complexity between the sexes Tables S1S2Figure 4and Figures S6, S7. Our reconstruction showed a strong phylogenetic signal where males of the Rhagovelia genus evolved an increasing number of secondary sexual traits Figure 4.

This pattern indicates substantial escalation of conflict in males Arnqvist and Rowe, ab ; Bergsten and Miller, ; Kuntner et al. In females, we detected the evolution of anti-grasping traits in a clade where males are the most armed Figure 4. However, these armaments do not show phylogenetic signal in females and we did not harassed correlation between male and female phenotypic complexities correlation test with phylogenetic independent contrast; rho: 0.

Based on our samples, these results suggest an on-going arms race between males and females in the Rhagovelia genus and more specifically in R. Figure 4. Comparison of male and female phenotypic harasssed. The phylogeny of our samples shows a higher complexity of male phenotypes, in terms of number of secondary sexual traits, hxrassed to outgroups left phylogeny.

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