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Mechanisms and Evidence of Genital Coevolution: the Roles of Natural Selection, Mate Choice, and Sexual Conflict

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Mechanisms and Evidence of Genital Coevolution: the Roles of Natural Selection, Mate Choice, and Sexual Conflict Downloaded from http://cshperspectives.cshlp.org/ on September 28, 2021 - Published by Cold Spring Harbor Laboratory Press Mechanisms and Evidence of Genital Coevolution: The Roles of Natural Selection, Mate Choice, and Sexual Conflict Patricia L.R. Brennan1,2 and Richard O. Prum3 1Departments of Psychology and Biology, University of Massachusetts, Amherst, MA 01003 2Organismic and Evolutionary Biology Graduate Program, University of Massachusetts, Amherst, MA 01003 3Department of Ecology and Evolutionary Biology and Peabody Museum of Natural History, Yale University, New Haven, CT 06520 Correspondence: [email protected] 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 coevo- lution is explicitly predicted byat 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. f all the evolutionary interactions between shown to covary in many taxa (Sota and Ku- Othe sexes, the mechanical interaction of bota 1998; Ilango and Lane 2000; Arnqvist and genitalia during copulation in species with in- Rowe 2002; Brennan et al. 2007; Ro¨nn et al. ternal fertilization is perhaps the most direct. 2007; Kuntner et al. 2009; Tatarnic and Cassis For this reason alone, coevolution between 2010; Cayetano et al. 2011; Evans et al. 2011, genital morphologies of males and females is 2013; Simmons and Garcı´a-Gonza´lez 2011; Yas- expected. Morphological and genetic compo- sin and Orgogozo 2013; and see examples in nents of male and female genitalia have been Table 1). Editors: William R. Rice and Sergey Gavrilets Additional Perspectives on The Genetics and Biology of Sexual Conflict available at www.cshperspectives.org Copyright # 2015 Cold Spring Harbor Laboratory Press; all rights reserved; doi: 10.1101/cshperspect.a017749 Cite this article as Cold Spring Harb Perspect Biol 2015;7:a017749 1 Downloaded from http://cshperspectives.cshlp.org/ P.L.R. Brennan and R.O. Prum 2 Table 1. Examples of coevolution found in a variety of taxa with emphasis on more recent literature and model systems Taxa Male structures Female structures Evidence Likely mechanism References Mollusks Land snails Spermatophore- Spermatophore-receiving Comparative among SAC or female choice Sauder and Hausdorf (Xerocrassa) producing organs organs species 2009 Satsuma Penis length Vagina length Character displacement Lock and key Kameda et al. 2009 Arthropods Arachnids (Nephilid Multiple Multiple Comparative among SAC Kuntner et al. 2009 spiders) species Pholcidae spiders Cheliceral apophysis Epigynal pockets Comparative (no Female choice Huber 1999 onSeptember28,2021-PublishedbyColdSpringHarborLaboratoryPress phylogenetic analysis) Harvestmen Hardened penes and Sclerotized pregenital Comparative among SAC Burns et al. 2013 (Opiliones) loss of nuptial gifts barriers species Millipedes Cite this article as Parafontaria Gonopod size Genital segment size Comparative in species Mechanical Sota and Tanabe 2010 tonominea complex incompatibility resulting from Intersexual selection Antichiropus variabilis Gonopod shape and Accesory lobe of the vulva and Functional copulatory Lock and key Wojcieszek and size distal projection morphology Simmons 2012 Cold Spring Harb Perspect Biol Crustacean Fiddler crabs, Uca Gonopode Vulva, vagina, and spermatheca Two-species comparison, Natural selection against Lautenschlager et al. shape correspondence fluid loss, lock and key, 2010 and sexual selection Hexapodes Odonates Clasping appendages Abdominal shape and Functional morphology, Lock and key via female Robertson and sensory hairs comparative among sensory system Paterson 1982; species McPeek et al. 2009 Insects Coleoptera: seed Spiny aedagus Thickened walls of Comparative among SAC Ro¨nn et al. 2007 2015;7:a017749 beetles copulatory duct species Callosobruchus: Damage inflicted Susceptibility to damage Full sib/half sib mating SAC Gay et al. 2011 Callosobruchus experiments maculatus Reduced spines No correlated response Experimental evolution SAC Cayetano et al. 2011 Continued Downloaded from http://cshperspectives.cshlp.org/ Cite this article as Table 1. Continued Taxa Male structures Female structures Evidence Likely mechanism References Carabid beetles Apophysis of the Vaginal appendix (pocket Cross-species matings Lock and key Sota and Kubota 1998; (Ohomopterus) endophallus attached to the vaginal Sasabi et al. 2010 Cold Spring Harb Perspect Biol apophysis) Dung beetle: Shape of the parameres Size and location of genital pits Experimental evolution Female choice Simmons and Garcı´a- Onthophagus in the aedagus Gonza´lez 2011 taurus Diptera: Drosophila Sclerotized spikes on Cavities with sclerotized Cross-species matings SAC Kamimura 2012 onSeptember28,2021-PublishedbyColdSpringHarborLaboratoryPress santomea and the aedagus platelets D. yakuba Drosophila Epandrial posterior Oviscapt pouches Comparative among SAC or female choice Yassin and Orgogozo melanogaster lobes species 2013 species complex 2015;7:a017749 Phallic spikes Oviscapt furrows Cercal teeth, phallic Uterine, vulval, and vaginal hook, and spines shields D. mauritiana and Posterior lobe of the Wounding of the female Mating with introgressed SAC Masly and Kamimura D. sechelia genital arch abdomen lines 2014 Stalk-eyed flies Genital process Common spermathecal duct Comparative among Female choice Kotrba et al. 2014 (Diopsidae) species and morphological Mechanisms of Genital Coevolution Tse-tse flies: Glossina Cercal teeth Female-sensing structures Experimental copulatory Female choice Bricen˜o and Eberhard pallidipes function 2009a,b Phelebotomine: Aedagal filaments, Spermathecal ducts length, Comparative among None specified Ilango and Lane 2000 sand flies aedagal sheaths base of the duct species Heteroptera: Bed bugs Piercing genitalia Spermalege (thickened Comparative among SAC Carayon 1966; Morrow (Cimiciidae) exosqueleton) species and Arnqvist 2003 Plant bugs Changes in male genital External female paragenitalia Comparative among SAC Tatarnic and Cassis (Coridromius) shape species 2010 Waterstriders Grasping appendages Antigrasping appendages Comparative among SAC Arnqvist and Rowe (Gerris sp.) species 2002 Gerris incognitus Grasping appendages Antigrasping appendages Comparative among SAC Perry and Rowe 2012 populations 3 Continued Downloaded from http://cshperspectives.cshlp.org/ P.L.R. Brennan and R.O. Prum 4 Table 1. Continued Taxa Male structures Female structures Evidence Likely mechanism References Bee assassins Aedagus Bursa copulatrix Comparative among None Forero et al. 2013 (Apiomerus) species Cave insects Male genital chamber Penis-like gynosome Comparative among Female competition (role Yoshizawa et al. 2014 (Psocodea), species reversal), coevolution Neotrogla SAC Butterflies Thickness of Signa: Sclerotized structure Comparative among SAC Sa´nchez and Cordero (Heliconiinae) spermatophore wall to break spermatophores species 2014 Fish onSeptember28,2021-PublishedbyColdSpringHarborLaboratoryPress Basking shark: Clasper claw Thick vaginal pads Morphological None Matthews 1950 Cetorhinus observation maximus Gambusia Gonopodial tips Genital papillae within Comparative among Strong character Langerhans 2011 openings species displacement Cite this article as Poecilia reticulata Gonopodium tip shape Female gonopore shape Comparative among SAC Evans et al. 2011 populations Reptiles Anoles Hemipene shape Vagina shape Shape correspondence, Sexual selection Ko¨hler et al. 2012 two species Cold Spring Harb Perspect Biol Several species Hemipene shape Vagina shape Shape correspondence Lock and key, female Pope 1941; Bo¨hme and choice, and SAC Ziegler 2009; King et al. 2009 Asiatic pit vipers Spininess in hemipenes Thickness of vagina wall Two-species comparison None Pope 1941 Garter snake: Basal hempene spine Vaginal muscular control Experimental SAC Friesen et al. 2014 Thamnophis sirtalis manipulation Birds Waterfowl Penis length Vaginal elaboration Comparative among SAC Brennan et al. 2007 species Tinamous Penis length/presence Vaginal elaboration Comparative among Female choice/natural PLR Brennan, K 2015;7:a017749 species selection Zyscowski, and RO Prum, unpubl. Continued Downloaded from http://cshperspectives.cshlp.org/ Cite this article as Table 1. Continued Taxa Male structures Female structures Evidence Likely mechanism References Cold Spring
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