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Something gone awry: unsolved mysteries in the evolution of asymmetric animal genitalia

In: Animal Biology
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  • 1 1Naturalis Biodiversity Center, Darwinweg 2, 2333 CR Leiden, The Netherlands
  • | 2 2Institute Biology Leiden, Leiden University, Sylviusweg 72, 2333 BE Leiden, The Netherlands
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The great diversity in genital shape and function across and within the animal phyla hamper the identification of specific evolutionary trends that stretch beyond the limits of the group under study. Asymmetry might be a trait in genital morphology that could play a unifying role in the evolutionary biology of genitalia. Here, I review the current knowledge on the taxonomic distribution, phylogenetic patterns, genetics, development, and ecology of asymmetric (chiral) genitalia. Asymmetric genitalia (male as well as female) have evolved from bilaterally symmetric ones (and sometimes vice versa), innumerous times in most animal taxa with internal fertilisation, and especially in Platyhelminthes, Arthropoda, Nematoda, and Chordata. In groups with asymmetric genitalia, chiral reversal (where species carry genitalia that are the mirror image of those in other, congeneric, species) is common, but antisymmetry (both mirror images present within a species) is rare. Although indications exist that, at least in insects, asymmetry evolves as a compensatory response to the evolution of male-dominant mating positions, many mysteries remain. Main questions are: (i) is genital asymmetry developmental-genetically linked with other (visceral, external) asymmetries? (ii) is genital asymmetry usually correlated with a change in mating position? (iii) is asymmetry more likely to evolve in response to cryptic female choice or sexually-antagonistic coevolution? (iv) why is antisymmetry so rare and how does chiral reversal evolve? Based on an overview of the taxonomic patterns, I advocate a research program that makes use of the simple, binary nature of left-right asymmetry to test hypotheses for its evolution with experimental and comparative methods. I also provide tables with full or summarised data on (a) genital asymmetry across all animal phyla with internal fertilisation; (b) genera with dextral as well as sinistral species; (c) species with dextral as well as sinistral individuals; (d) genera with symmetric as well as asymmetric species; (e) species with symmetric as well as asymmetric individuals.

Abstract

The great diversity in genital shape and function across and within the animal phyla hamper the identification of specific evolutionary trends that stretch beyond the limits of the group under study. Asymmetry might be a trait in genital morphology that could play a unifying role in the evolutionary biology of genitalia. Here, I review the current knowledge on the taxonomic distribution, phylogenetic patterns, genetics, development, and ecology of asymmetric (chiral) genitalia. Asymmetric genitalia (male as well as female) have evolved from bilaterally symmetric ones (and sometimes vice versa), innumerous times in most animal taxa with internal fertilisation, and especially in Platyhelminthes, Arthropoda, Nematoda, and Chordata. In groups with asymmetric genitalia, chiral reversal (where species carry genitalia that are the mirror image of those in other, congeneric, species) is common, but antisymmetry (both mirror images present within a species) is rare. Although indications exist that, at least in insects, asymmetry evolves as a compensatory response to the evolution of male-dominant mating positions, many mysteries remain. Main questions are: (i) is genital asymmetry developmental-genetically linked with other (visceral, external) asymmetries? (ii) is genital asymmetry usually correlated with a change in mating position? (iii) is asymmetry more likely to evolve in response to cryptic female choice or sexually-antagonistic coevolution? (iv) why is antisymmetry so rare and how does chiral reversal evolve? Based on an overview of the taxonomic patterns, I advocate a research program that makes use of the simple, binary nature of left-right asymmetry to test hypotheses for its evolution with experimental and comparative methods. I also provide tables with full or summarised data on (a) genital asymmetry across all animal phyla with internal fertilisation; (b) genera with dextral as well as sinistral species; (c) species with dextral as well as sinistral individuals; (d) genera with symmetric as well as asymmetric species; (e) species with symmetric as well as asymmetric individuals.

Introduction

Until three decades ago, the now blossoming field of animal genital evolution (Cordero and Eberhard, 2003; Leonard and Córdoba-Aguilar, 2010; Joly and Schmitt, 2010) did not yet exist. However, seminal empirical (Waage, 1979) and synthetic (Eberhard, 1985) publications, aided by developments in sexual selection theory (Eberhard, 1996; Rice, 1996; Arnqvist, 1998; Rowe et al., 2003; Hosken and Stockley, 2004) helped create a framework that allowed the field to develop rapidly. Today, bibliographic tools reveal a sharply rising output of over one hundred papers per year on the evolution of genitalia, which is beginning to approach the publication rates in the evolutionary biology of plant reproductive structures.

The field has benefited greatly from the wealth of available knowledge on morphological diversity in genitalia, brought together by taxonomists for those groups in which genitalia are routinely used in classification and identification (Eberhard, 1985). At the same time, however, the great diversity in genital shape and function across and within the animal phyla hamper the identification of specific evolutionary trends that stretch beyond the limits of the group under study. For example, the evolutionary processes involved in diversification of penile spines have been studied within, e.g., primates, Lepidoptera, Callosobruchus beetles and the melanogaster-group of Drosophila (Stockley, 2002; Kamimura, 2007; Rönn et al., 2007; Cordero and Miller, 2012), but the great disparity in morphological derivation prevent generalization across these groups.

One of the structural aspects of genitalia that can be studied in a meaningful way across animal taxa is asymmetry. This is a common and widespread feature in the genitalia of many animals (Ludwig, 1932; Huber et al., 2007; Kamimura and Iwase, 2010; Schilthuizen, 2011). At least seven (not all mutually exclusive) explanations have been put forward for the origin of asymmetry in genitalia (Huber et al., 2007; Schilthuizen, 2007), namely (i) morphological compensation for selected changes in mating position; (ii) male-female sexual arms races; (iii) cryptic female choice for asymmetric male genitalia; (iv) different functions for the left and right side; (v) one-sided reduction to save space and resources; (vi) functional constraints: to function properly, the separate parts of the genitalia need to connect in an asymmetric fashion; (vii) efficient packing: internal genitalia need to fit among other, asymmetric, organs in the body cavity. At least the first three of these may be of relatively general applicability.

Palmer (1996) has highlighted the relevance of studying partial or whole-body asymmetry in otherwise bilaterally symmetric animals. Not only have asymmetric shapes evolved repeatedly, in a wide variety of organ systems, and in representatives of almost all lineages of the Bilateria, but, more importantly, their “binary switch” nature allows generalizations that transcend the limits of individual taxa (Palmer, 2004). In this paper, I will advocate a research program that makes use of these benefits in investigating structural asymmetry in the evolution of animal genitalia.

Definitions and terminology

Most, if not all, bilaterian animals carry certain morphological traits that are conspicuously asymmetric across the plane of body symmetry (I will not discuss fluctuating asymmetry, FA, the subtle variation around a mean of perfect symmetry; Van Valen, 1962). Well-known examples of conspicuous asymmetry include the orientation of the internal organs of mammals, the unequal claws in crabs and lobsters, the torsion of the head in flatfishes, and the coiling of much of the body in Gastropoda (Vermeij, 1975; Policansky, 1978; Okada et al., 1999; Schilthuizen and Davison, 2005; Friedman, 2008; Palmer, 2009). I will adopt Palmer’s (2005) terminology, as follows. The two mirror images of an asymmetric (chiral) form are termed enantiomorphs. I will identify these as dextral and sinistral, although these terms do not provide any information about the actual shapes, except in the case of helical structures. In directional asymmetry (DA), only one of the two enantiomorphs is present (with the exception of very rare mutants, usually ≪1%). In pure antisymmetry (AS), both enantiomorphs are present at equal frequencies. In biased AS, the more common enantiomorph is present at a frequency of more than 50% but less than 90%. I will also discuss a few cases in which symmetry and conspicuous asymmetry occur within the same species, which I term DA/SYM dimorphism.

Here, I follow Eberhard (1985) and Huber et al. (2007) in defining male genitalia as “structures that are inserted in the female or that hold her near her gonopore during sperm transfer”, and female genitalia as “those parts of the female reproductive tract that make direct contact with male genitalia or male products (sperm, spermatophores) during or immediately following copulation”. I will limit myself to “structural asymmetry”, i.e., asymmetry of genital structures that lie in the body’s mid-plane or morphological dissimilarity between the left and right member of paired structures. Although possibly evolutionarily a springboard for structural asymmetry (Palmer, 2006), I will not discuss behavioural laterality of otherwise symmetric paired structures; e.g., handed penis use in the paired penises in Dermaptera (Kamimura and Iwase, 2010); removal of one pedipalp in male theridiid spiders (Knoflach and van Harten, 2000) and asymmetric positioning in the body cavity of otherwise bilaterally symmetric genital structures (e.g., rotation of the penis in leaf beetles [Verma and Kumar, 1972; Tiwary and Verma, 1989]).

Taxonomic distribution

Given the above definition of genitalia, the animal phyla referred to here are those in which direct contact between males and females is part of reproduction. This includes at least ten phyla, of which Platyhelminthes, Arthropoda, Nematoda, and Chordata display the most widespread genital asymmetry. This is listed in table S1 (online supplementary material), and a few striking examples are given below and in fig. 1.

Figure 1.
Figure 1.

Pairwise examples of animal species with asymmetric (top row) male genitalia and their counterparts in related symmetric species (bottom row). (A) Limnodrilus cervix Brinckhurst, 1963: Tubificidae: Oligochaeta: Annelida (penis, after Stimpson et al., 1982); (B) Limnodrilus hoffmeisteri Claparède, 1862: Tubificidae: Oligochaeta: Annelida (penis, after Stimpson et al., 1982); (A-B) note, however, that the penes in Limnodrilus are paired; (C) Metagonia mariguitarensis (González-Sponga, 1998): Pholcidae: Araneae: Arthropoda (right and left palp, after Huber, 2000); (D) Metagonia tingo Huber, 2000: Pholcidae: Aranaea: Arthropoda (left and right palp, after Huber, 2000); (E) Sus scrofa L. 1758: Suidae: Mammalia: Chordata (penis, after Nickel-Schummer-Seiferle, 1960, in Prasad, 1970); (F) Dama dama (L. 1758): Cervidae: Mammalia: Chordata (penis, after Mandowsky, 1927, in Prasad, 1970); (G) Gieysztoria dodgei (Graff, 1911): Dalyelliidae: Rhabdocoela: Platyhelminthes (genital armature, after Graff, 1911); (H) Microdalyellia fairchildi (Graff, 1911): Dalyelliidae: Rhabdocoela: Platyhelminthes (genital armature, after Graff, 1911); (I) Tetrameres spirospiculum Pinto and Vicente, 1995: Tetrameridae: Spirurida: Nematoda (spicules, after Pinto and Vicente, 1995); (J) Oswaldocruzia tcheprakovae Ben Slimane and Durette-Desset, 1996: Molineidae: Strongylida: Nematoda (spicules, after Ben Slimane and Durette-Desset, 1996). All figured in ventrodorsal view, except C and D, which are figured in retrolateral and prolateral view, respectively.

Citation: Animal Biology 63, 1 (2013) ; 10.1163/15707563-00002398

In Arthropoda, genital asymmetry is extremely rare in Aranaea, present in a few groups within the Acari and Crustacea (especially Copepoda), relatively common in Opiliones, and exceedingly common in Insecta (table S1). Huber et al. (2007) summarise the insect data as follows: “In some insect orders or superorders, genital asymmetry is in the groundplan (e.g. Dictyoptera, Embiidina, Phasmatodea), in others it has evolved multiple times convergently (e.g. Coleoptera, Diptera, Heteroptera, Lepidoptera).” As