Escalation and Morphological Constraints of Antagonistic Armaments in Water Striders Antonin Jean Johan Crumière, David Armisen, Aïdamalia Vargas-Lowman, Martha Kubarakos, Felipe Ferraz Figueiredo Moreira, Abderrahman Khila To cite this version: Antonin Jean Johan Crumière, David Armisen, Aïdamalia Vargas-Lowman, Martha Kubarakos, Felipe Ferraz Figueiredo Moreira, et al.. Escalation and Morphological Constraints of Antagonistic Arma- ments in Water Striders. Frontiers in Ecology and Evolution, Frontiers Media S.A, 2019, 7, pp.12. 10.3389/fevo.2019.00215. hal-02392029 HAL Id: hal-02392029 https://hal.archives-ouvertes.fr/hal-02392029 Submitted on 25 May 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution - NonCommercial| 4.0 International License ORIGINAL RESEARCH published: 18 June 2019 doi: 10.3389/fevo.2019.00215 Escalation and Morphological Constraints of Antagonistic Armaments in Water Striders Antonin Jean Johan Crumière 1†, David Armisén 1†, Aïdamalia Vargas-Lowman 1, Martha Kubarakos 1†, Felipe Ferraz Figueiredo Moreira 2 and Abderrahman Khila 1* Edited by: 1 Institut de Génomique Fonctionnelle de Lyon, CNRS UMR 5242, Ecole Normale Supérieure de Lyon, Université de Lyon, Jingchun Li, Université Claude Bernard Lyon 1, Lyon, France, 2 Laboratório de Biodiversidade Entomológica, Instituto Oswaldo Cruz, University of Colorado Boulder, Fundação Oswaldo Cruz, Rio de Janeiro, Brazil United States Reviewed by: Sexual conflict may result in the escalating coevolution of sexually antagonistic traits. Jessica Goodheart, University of California, Santa Barbara, However, our understanding of the evolutionary dynamics of antagonistic traits and their United States role in association with sex-specific escalation remains limited. Here we study sexually Luigi Caputi, Stazione Zoologica Anton Dohrn, Italy antagonistic coevolution in a genus of water striders called Rhagovelia. We identified *Correspondence: a set of male grasping traits and female anti-grasping traits used during pre-mating Abderrahman Khila struggles and show that natural variation of these traits is associated with variation in [email protected] mating performance in the direction expected for antagonistic coevolution. Phylogenetic †Present Address: mapping detected signal of escalation of these sexually antagonistic traits suggesting Antonin Jean Johan Crumière, an ongoing arms race. Moreover, their escalation appears to be influenced by a trade- Section for Ecology and Evolution, Department of Biology, University of off with dispersal through flight in both sexes. Altogether our results highlight how Copenhagen, Copenhagen, Denmark sexual interactions and natural selection may have shaped sex-specific antagonistic David Armisén, INRA-Université Clermont-Auvergne, trait coevolution. UMR 1095 GDEC, Clermont-Ferrand, Keywords: sexual conflict, antagonistic armaments, coevolution, water striders, sexual dimorphism France Martha Kubarakos, Department of Pharmaceutical Sciences, University of Toronto, INTRODUCTION Toronto, ON, Canada The evolutionary interests of males and females in reproductive interactions often diverge, leading Specialty section: to the coevolution of sexually antagonistic traits that are favored in one sex at a fitness cost to the This article was submitted to other (Arnqvist and Rowe, 2005). Females possess a limited number of eggs and pay increasing costs Coevolution, for multiple mating (Rowe et al., 1994; Arnqvist and Rowe, 2005). On the other hand, males are a section of the journal favored to mate repeatedly because increased mating rate in males results in increased fitness (Rowe Frontiers in Ecology and Evolution et al., 1994; Arnqvist and Rowe, 2005). These opposing interests during mating interactions cause Received: 09 March 2019 sexual conflict over mating rate (Arnqvist and Rowe, 2005). In this specific case, sexual antagonism Accepted: 23 May 2019 drives the evolution of armaments whereby grasping traits allowing males to persist and increase Published: 18 June 2019 their mating success are often matched by the evolution of anti-grasping traits in females improving Citation: their ability to resist and thus escape fitness costs associated with superfluous mating events Crumière AJJ, Armisén D, (Weigensberg and Fairbairn, 1996; Arnqvist and Rowe, 2002b). The repeated evolution of such sex- Vargas-Lowman A, Kubarakos M, specific armaments can lead to episodes of escalation and ultimately arms race (Arnqvist and Rowe, Moreira FFF and Khila A (2019) 1995, 2002a; Pennell and Morrow, 2013). Sex chromosome evolution (Dean et al., 2012; Pennell and Escalation and Morphological Constraints of Antagonistic Morrow, 2013), sex biased gene expression (Snook et al., 2010; Mank et al., 2013; Mank, 2017) and Armaments in Water Striders. intra- and inter-locus sexual conflict (Rowe and Day, 2006; Bonduriansky and Chenoweth, 2009; Front. Ecol. Evol. 7:215. Crumiere and Khila, 2019), are expected to drive the divergence of the sexes, often resulting in doi: 10.3389/fevo.2019.00215 striking cases of sexual dimorphism (Rowe and Day, 2006; Bonduriansky and Chenoweth, 2009). Frontiers in Ecology and Evolution | www.frontiersin.org 1 June 2019 | Volume 7 | Article 215 Crumière et al. Water Strider Antagonistic Armament Coevolution The dynamics of morphological co-evolution of sexually femur is entirely occupied by muscles (Figure S1), suggesting antagonistic traits has attracted much attention (Arnqvist and that thicker femurs have the potential to apply stronger grip Rowe, 2002a; Bergsten and Miller, 2007; Kuntner et al., 2009) force. In females, winged morphs possess a prominent spike-like and water striders have been widely used as a model to study projection of the pronotun (Figure 1H’; Polhemus, 1997) that sexual dimorphism and antagonistic co-evolution in the context is not found in wingless females (Figure 1C’) or winged males of sexual conflict (Arnqvist, 1992; Arnqvist and Rowe, 1995; (Figure 1H; Polhemus, 1997). Wingless females have a narrow- Weigensberg and Fairbairn, 1996). Despite the rich diversity shaped abdomen (Figure 2B) that can be even more pronounced of this group of semiaquatic insects, the vast majority of in some species such as Rhagovelia obesa (Figure 2C). We these studies have focused on the Gerridae family (Insecta, have never observed winged females with narrow abdomen Heteroptera, Gerromorpha, Veliidae) (Arnqvist, 1992; Arnqvist or wingless females with pronotum projection indicating that and Rowe, 1995, 2002a; Weigensberg and Fairbairn, 1996). these two traits are mutually exclusive (Figures 2A,B). This Here, we investigated the evolution of sexual dimorphism observation suggests that morph-specific strategies to reduce in the tropical genus Rhagovelia from the Veliidae family mating frequency have evolved in Rhagovelia females. (Insecta, Heteroptera, Gerromorpha, Veliidae) (Andersen, 1982; Polhemus, 1997; Moreira and Ribeiro, 2009). In this genus, Mating Behavior in Rhagovelia antilleana sexual dimorphism is particularly dramatic with both sexes often Pre-mating interactions in R. antilleana include vigorous bearing morphological traits reminiscent to those usually found struggles between males and females, characteristic of sexual in species with strong sexual conflict (Andersen, 1982; Polhemus, conflict over mating rate (Arnqvist and Rowe, 1995, 2005; Khila 1997; Arnqvist and Rowe, 2005; Moreira and Ribeiro, 2009). et al., 2012). Behavioral quantification revealed that both winged However, the process of sexual selection; i.e., male competition, and wingless males approach females preferably on the side and mate choice or sexual conflict over mating rate, driving the back by grasping female’s mid- and rearlegs (Figure S2A). sexual dimorphism in Rhagovelia is unknown (Andersson, We did not detect a significant male preference for winged or 1994; Arnqvist and Rowe, 2005). Through morphological and wingless morphs or any differences in the frequency of mating behavioral observations, we identified a large set of potentially events related to the overall numbers of pre-mating interactions sexually antagonistic armaments in the Rhagovelia genus and across female morphs (Figures S2B–D). When mounted, males tested their role during sexual interactions in a representative use the sex combs to clasp the pronotum of the female and species called Rhagovelia antilleana (Andersen, 1982; Polhemus, tighten the grip on her legs using their modified rearlegs 1997; Moreira and Ribeiro, 2009). We then tested how variation (Supplementary Video 1). Females vigorously shake their body in sexually antagonistic traits affects male and female success and perform repeated somersaults, which frequently result in during sexual interactions. We show that this variation is rejecting the male (Supplementary Video 2). The struggles are associated with trade-offs with flight capability and egg storage. vigorous and their duration is typically 0.68 ± 0.99 s in average, Finally, we used phylogenetic reconstruction of male and but