Canadian Journal of Zoology Morphology of genitalia and non-genitalic contact structures in Trouessartia spp. feather mites (Astigmata: Analgoidea: Trouessartiidae): is there evidence of correlated evolution between the sexes? Journal: Canadian Journal of Zoology Manuscript ID cjz-2019-0291.R1 Manuscript Type: Article Date Submitted by the 23-Jun-2020 Author: Complete List of Authors: Byers, Kaylee; The University of British Columbia, Interdisciplinary Studies; Canadian Wildlife Health Cooperative, Animal Health Centre Proctor, H.C.;Draft University of Alberta, Department of Biological Sciences Is your manuscript invited for consideration in a Special Zoological Endeavors Inspired by A. Richard Palmer Issue?: Acariformes, COEVOLUTION < Discipline, feather mite, GENITALIA < Keyword: Organ System, Trouessartia, sexual conflict, sexual dimorphism https://mc06.manuscriptcentral.com/cjz-pubs Page 1 of 45 Canadian Journal of Zoology Morphology of genitalia and non-genitalic contact structures in Trouessartia spp. feather mites (Astigmata: Analgoidea: Trouessartiidae): is there evidence of correlated evolution between the sexes?1 Kaylee A. Byers1a and Heather C. Proctor1 1 Department of Biological Sciences, University of Alberta, Edmonton, AB, Canada Emails: Kaylee Byers: [email protected] Heather Proctor: [email protected] Correspondence: Kaylee Byers, email: [email protected], phone: 778-980-9948 Department of Interdisciplinary Studies University of British Columbia 270, 2357 Main Mall, H.R. MacMillan Building Vancouver, BC, V6T 1Z4 a Current affiliations for Kaylee Byers are: Department of Interdisciplinary Studies, University of British Columbia, Vancouver, BC, Canada Biodiversity Research Centre, University of British Columbia, Vancouver, BC, Canada 1This article is one of a series of invited papers arising from the symposium “Zoological Endeavours Inspired by A. Richard Palmer” that was co-sponsored by the Canadian Society of Zoologists and the Canadian Journal of Zoology and held during the Annual Meeting of the Canadian Society of Zoologists at the University of Windsor, Windsor, Ontario, 14–16 May 2019. 1 https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 2 of 45 Morphology of genitalia and non-genitalic contact structures in Trouessartia spp. feather mites (Astigmata: Analgoidea: Trouessartiidae): is there evidence of correlated evolution between the sexes? Kaylee A. Byers and Heather C. Proctor Abstract Positive correlations between the shapes of male and female sexual structures can be interpreted as cooperative or as combative. In the feather mite genus Trouessartia Canestrini, 1899, the spermaducts of females range from entirely internal to extending externally for varying lengths, while male primary genitalia range from gracile to massive. Males also possess a pair of adanal suckers used to hold onto the dorsalDraft surface of the female during copulation. In the area of this attachment, females exhibit ornamentation and have strongly developed dorsal setae (setae h1), which we hypothesized serve to weaken the male’s hold during copulation. In male and female Trouessartia from 51 bird species, we compared female external spermaduct length and male genitalic ‘massiveness’ and explored whether patterns of female dorsal ornamentation and/or h1 seta size correlate with male adanal sucker size. Our results indicate that females with longer external spermaducts are associated with males with relatively massive genitalia. However, we found no significant relationship between male adanal sucker size and female ornamentation or h1 seta size. Further information regarding how the genitalia interact during sperm transfer is necessary to interpret correlations in genitalia size and strong intersexual differences in dorsal ornamentation and seta size in Trouessartia. 2 https://mc06.manuscriptcentral.com/cjz-pubs Page 3 of 45 Canadian Journal of Zoology Keywords: Acariformes, coevolution, feather mite, genitalia, Trouessartia, sexual conflict, sexual dimorphism Introduction In sexual species, both males and females have a vested interest in the fitness gained from the successful completion of mating; however, reproductive investment is often disproportionate between the sexes (Bateman 1948). As a result, the sex with higher gametic or parental investment will often be more selective of its mating partner (Parker et al. 1979). Females commonly invest more in their offspring than do males (e.g., anisogamy, Bateman 1948); given this, females are often the limitingDraft sex (Trivers 1972). This differential investment between the sexes can promote sexual conflict, whereby each sex acts to further its own interests. In some cases this struggle to gain control of fertilization can be at the cost of the opposite sex (Parker et al. 1979; Arnqvist and Rowe 2005; Rönn et al. 2007; Madjidian et al. 2012). Costs to females from undesired matings include reduction in their own reproductive success (Alexander et al. 1997), damage to the reproductive tract (Siva-Jothy 2006) and increased predation (Rowe 1994). Male genitalia and structures associated with holding or restraining females are among the most rapidly evolving features in internally fertilizing animals and are often more interspecifically variable than female genitalia (Eberhard 1985; but see Simmons and Fitzpatrick 2019). This rapid diversification in male genitalia is hypothesized to arise via selection to reduce 3 https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 4 of 45 hybridization (lock-and-key, Masly 2012) or via sexual selection (Eberhard 2010a) acting through cryptic female choice (Eberhard 1985), male-male competition for fertilization (sperm competition, Parker 1970), or sexually antagonistic coevolution (Arnqvist and Rowe 2005). The importance of selection against hybridization has fewer proponents today than when it was first suggested in the 1800s (Masly 2012), and the majority of current studies of genitalic evolution focus on disentangling the various sexual selection hypotheses. Although these hypotheses are not always mutually exclusive (Hosken and Stockley 2004; Eberhard 2010b), there is growing evidence of the importance of conflict between the sexes in the evolution of reproductive features. Sexually antagonistic coevolutionDraft in reproductive structures has been documented in both vertebrates (Brennan et al. 2007) and invertebrates (Arnqvist and Rowe 2005; Koene and Schulenburg 2005; Perry and Rowe 2012; Bilton et al. 2016) and has been associated with traumatic insemination and harmful male genitalia in arthropods (Rönn et al. 2007; Tatarnic and Cassis 2010; Kamimura 2012; Dougherty et al. 2017). In addition to sexually antagonistic coevolution in genitalic structures, sexual conflict may also influence non-genitalic contact structures involved in mate acquisition (Arnqvist and Rowe 2002a; Crumière et al. 2019). These structures can range from the sucker-like bursa of male nematodes (Ahmad and Jairajpuri 1981) to the cerci of male dragonflies (McPeek et al. 2009). Non- genitalic contact devices employed by males to grasp females often correspond to the dimensions of the female’s ‘receptive’ structures (Arnqvist and Rowe 4 https://mc06.manuscriptcentral.com/cjz-pubs Page 5 of 45 Canadian Journal of Zoology 2002a; Huber 2003; McPeek et al. 2009; but see Byers and Proctor 2014). An excellent example of antagonistic coevolution in grasping structures occurs in some diving beetles (Coleoptera: Dytiscidae), where males possess tarsal suction cups to grasp females and females have evolved modified dorsal indentations (macropunctures) and setose furrows at these areas that weaken the male’s ability to retain a strong grip (Bergsten and Miller 2007; Karlsson Green et al. 2013; Bilton et al. 2016). In response, males have evolved even more elaborate suction cup morphologies to counteract these female modifications. Similar patterns have been reported in the male grasping and female anti- grasping structures (dorsally pointing spines) of water striders (Hemiptera: Gerridae) (Arnqvist and Rowe 2002Draftb). Correlations between genitalic structures are often difficult to test due to the primarily internal nature of most female genitalia. However, some parts of the female genitalia of spiders and feather mites (Acari: Astigmata) are sclerotized (Proctor 2003; Kuntner et al. 2016) and are readily visible through the body wall in cleared or slide-mounted specimens, making them ideal for studying genitalic traits. Although the genitalia of female spiders have been the focus of a fair amount of research on sexual selection (e.g., Eberhard 2004; Huber et al. 2005; Kuntner et al. 2009; Kuntner et al. 2016), feather mites have been almost entirely overlooked in studies of genitalic evolution in both sexes (but see Klimov et al. 2017). Similar to other astigmatan mites, most male feather mites possess a sclerotized tubular or rod-shaped aedeagus (copulatory organ), which females of most species receive in their copulatory pore. This 5 https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 6 of 45 pore connects to the female’s internal sclerotized spermaduct that in turn leads to the spermatheca (Popp 1967; Proctor 2003). In some species of Astigmata, the spermaduct has both an internal section and an external section that extends outside of the female’s body (see Klimov and Sidorchuk 2011). Members of the vane-dwelling feather mite genus Trouessartia Canestrini, 1899 (Analgoidea: Trouessartiidae)