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Genital coevolution between the sexes is expected to be common because of the direct interaction between male and female genitalia during copulation. Here we review the diverse mechanisms of genital coevolution that include natural selection, female mate choice, male–male competition, and how their interactions generate sexual conflict that can lead to sexually antagonistic coevolution. Natural selection on genital morphology will result in size coevolution to allow for copulation to be mechanically possible, even as other features of genitalia may reflect the action of other mechanisms of selection. Genital coevolution is explicitly predicted by at least three mechanisms of genital evolution: lock and key to prevent hybridization, female choice, and sexual conflict. Although some good examples exist in support of each of these mechanisms, more data on quantitative female genital variation and studies of functional morphology during copulation are needed to understand more general patterns. A combination of different approaches is required to continue to advance our understanding of genital coevolution. Knowledge of the ecology and behavior of the studied species combined with functional morphology, quantitative morphological tools, experimental manipulation, and experimental evolution have been provided in the best-studied species, all of which are invertebrates. Therefore, attention to vertebrates in any of these areas is badly needed.Of all the evolutionary interactions between the sexes, the mechanical interaction of genitalia during copulation in species with internal fertilization is perhaps the most direct. For this reason alone, coevolution between genital morphologies of males and females is expected. Morphological and genetic components of male and female genitalia have been shown to covary in many taxa (Sota and Kubota 1998; Ilango and Lane 2000; Arnqvist and Rowe 2002; Brennan et al. 2007; Rönn et al. 2007; Kuntner et al. 2009; Tatarnic and Cassis 2010; Cayetano et al. 2011; Evans et al. 2011, 2013; Simmons and García-González 2011; Yassin and Orgogozo 2013; and see examples in Taxa Male structures Female structures Evidence Likely mechanism References Mollusks Land snails (Xerocrassa) Spermatophore-producing organs Spermatophore-receiving organs Comparative among species SAC or female choice Sauder and Hausdorf 2009 Satsuma Penis length Vagina length Character displacement Lock and key Kameda et al. 2009 Arthropods Arachnids (Nephilid spiders) Multiple Multiple Comparative among species SAC Kuntner et al. 2009 Pholcidae spiders Cheliceral apophysis Epigynal pockets Comparative (no phylogenetic analysis) Female choice Huber 1999 Harvestmen (Opiliones) Hardened penes and loss of nuptial gifts Sclerotized pregenital barriers Comparative among species SAC Burns et al. 2013 Millipedes Parafontaria tonominea Gonopod size Genital segment size Comparative in species complex Mechanical incompatibility resulting from Intersexual selection Sota and Tanabe 2010 Antichiropus variabilis Gonopod shape and size Accesory lobe of the vulva and distal projection Functional copulatory morphology Lock and key Wojcieszek and Simmons 2012 Crustacean Fiddler crabs, Uca Gonopode Vulva, vagina, and spermatheca Two-species comparison, shape correspondence Natural selection against fluid loss, lock and key, and sexual selection Lautenschlager et al. 2010 Hexapodes Odonates Clasping appendages Abdominal shape and sensory hairs Functional morphology, comparative among species Lock and key via female sensory system Robertson and Paterson 1982; McPeek et al. 2009 Insects Coleoptera: seed beetles Spiny aedagus Thickened walls of copulatory duct Comparative among species SAC Rönn et al. 2007 Callosobruchus: Callosobruchus maculatus Damage inflicted Susceptibility to damage Full sib/half sib mating experiments SAC Gay et al. 2011 Reduced spines No correlated response Experimental evolution SAC Cayetano et al. 2011 Carabid beetles (Ohomopterus) Apophysis of the endophallus Vaginal appendix (pocket attached to the vaginal apophysis) Cross-species matings Lock and key Sota and Kubota 1998; Sasabi et al. 2010 Dung beetle: Onthophagus taurus Shape of the parameres in the aedagus Size and location of genital pits Experimental evolution Female choice Simmons and García-González 2011 Diptera: Drosophila santomea and D. yakuba Sclerotized spikes on the aedagus Cavities with sclerotized platelets Cross-species matings SAC Kamimura 2012 Drosophila melanogaster species complex Epandrial posterior lobes
Oviscapt pouches Comparative among species SAC or female choice Yassin and Orgogozo 2013 Phallic spikes Oviscapt furrows Cercal teeth, phallic hook, and spines Uterine, vulval, and vaginal shields D. mauritiana and D. sechelia Posterior lobe of the genital arch Wounding of the female abdomen Mating with introgressed lines SAC Masly and Kamimura 2014 Stalk-eyed flies (Diopsidae) Genital process Common spermathecal duct Comparative among species and morphological Female choice Kotrba et al. 2014 Tse-tse flies: Glossina pallidipes Cercal teeth Female-sensing structures Experimental copulatory function Female choice Briceño and Eberhard 2009a,b Phelebotomine: sand flies Aedagal filaments, aedagal sheaths Spermathecal ducts length, base of the duct Comparative among species None specified Ilango and Lane 2000 Heteroptera: Bed bugs (Cimiciidae) Piercing genitalia Spermalege (thickened exosqueleton) Comparative among species SAC Carayon 1966; Morrow and Arnqvist 2003 Plant bugs (Coridromius) Changes in male genital shape External female paragenitalia Comparative among species SAC Tatarnic and Cassis 2010 Waterstriders (Gerris sp.) Grasping appendages Antigrasping appendages Comparative among species SAC Arnqvist and Rowe 2002 Gerris incognitus Grasping appendages Antigrasping appendages Comparative among populations SAC Perry and Rowe 2012 Bee assassins (Apiomerus) Aedagus Bursa copulatrix Comparative among species None Forero et al. 2013 Cave insects (Psocodea), Neotrogla Male genital chamber Penis-like gynosome Comparative among species Female competition (role reversal), coevolution SAC Yoshizawa et al. 2014 Butterflies (Heliconiinae) Thickness of spermatophore wall Signa: Sclerotized structure to break spermatophores Comparative among species SAC Sánchez and Cordero 2014 Fish Basking shark: Cetorhinus maximus Clasper claw Thick vaginal pads Morphological observation None Matthews 1950 Gambusia Gonopodial tips Genital papillae within openings Comparative among species Strong character displacement Langerhans 2011 Poecilia reticulata Gonopodium tip shape Female gonopore shape Comparative among populations SAC Evans et al. 2011 Reptiles Anoles Hemipene shape Vagina shape Shape correspondence, two species Sexual selection Köhler et al. 2012 Several species Hemipene shape Vagina shape Shape correspondence Lock and key, female choice, and SAC Pope 1941; Böhme and Ziegler 2009; King et al. 2009 Asiatic pit vipers Spininess in hemipenes Thickness of vagina wall Two-species comparison None Pope 1941 Garter snake: Thamnophis sirtalis Basal hempene spine Vaginal muscular control Experimental manipulation SAC Friesen et al. 2014 Birds Waterfowl Penis length Vaginal elaboration Comparative among species SAC Brennan et al. 2007 Tinamous Penis length/presence Vaginal elaboration Comparative among species Female choice/natural selection PLR Brennan, K Zyscowski, and RO Prum, unpubl. Mammals Marsupials Bifid penis Two lateral vaginae Shape correspondence None Renfree 1987 Equidna Bifid penis with four rosettes Single vagina splits into two uteri Shape correspondence None Augee et al. 2006; Johnston et al. 2007 Insectivores: Short-tailed shrew: Blarina brevicauda S-shaped curve of the erect penis Coincident curve in the vagina Shape correspondence None Bedford et al. 2004 Common tenrec: Tenrec caudatus Filiform penis (up to 70% of the male’s body length) Internal circular folds in the vagina Length correspondence None Bedford et al. 2004 Rodents: Cape dune mole: Bathyergus suillus Penis and baculum length Vaginal length Allometric relationships within species None Kinahan et al. 2007 Australian hopping mice (Notomys) Spiny penis Derived distal region in the vagina Morphological observation and two-species comparison Copulatory lock Breed et al. 2013 Pig: Sus domesticus Filiform penis end Cervical ridges Artificial insemination Female choice Bonet et al. 2013 Primates: Macaca arctoides Long and filamentous glans Vestibular colliculus (fleshy fold) that partially obstructs the entrance to the vagina Shape correspondence and comparison with close relatives None Fooden 1967