Consequences of Inbreeding Depression Due to Sex-Linked Loci for the Maintenance of Males and Outcrossing in Branchiopod Crustaceans
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Genet. Res., Camb. (2008), 90, pp. 73–84. f 2008 Cambridge University Press 73 doi:10.1017/S0016672307008981 Printed in the United Kingdom Consequences of inbreeding depression due to sex-linked loci for the maintenance of males and outcrossing in branchiopod crustaceans JOHN R. PANNELL* Department of Plant Sciences, South Parks Road, University of Oxford, Oxford OX1 3RB, UK (Received 10 August 2007 and in revised form 27 October 2007) Summary Androdioecy, where males co-occur with hermaphrodites, is a rare sexual system in plants and animals. It has a scattered phylogenetic distribution, but it is common and has persisted for long periods of evolutionary time in branchiopod crustaceans. An earlier model of the maintenance of males with hermaphrodites in this group, by Otto et al. (1993), considered the importance of male–hermaphrodite encounter rates, sperm limitation, male versus hermaphrodite viability and inbreeding depression suffered by selfed progeny. Here I advance this model in two ways: (1) by exploring the conditions that would allow the invasion of hermaphrodites into a dioecious population and that of females into an androdioecious population; and (2) by incorporating a term that accounts for the potential effects of genetic load linked to a dominant hermaphrodite- determining allele in androdioecious populations. The new model makes plausible sense of observations made in populations of the species Eulimnadia texana, one of a number of related species whose common ancestor evolved hermaphroditism (and androdioecy) from dioecy. In particular, it offers an explanation for the long evolutionary persistence of androdioecy in branchiopods and suggests reasons for why dioecy has not re-evolved in the clade. Finally, it provides a rather unusual illustration of the implications of the degeneration of loci linked to a sex-determining locus. 1. Introduction et al., 1999; Sakai, 2001; reviewed in Pannell, 2002; Weeks et al., 2006a). Although androdioecy must still Androdioecy, the occurrence of males and hermaphro- count as exceedingly rare, its discovery has led to dites in a population, is a rare sexual system in both new insights regarding selective factors that maintain plants and animals. The term was coined by Darwin combined versus separate sexes. In particular, while (1877), who considered it as a possible path from androdioecy may be difficult to evolve from her- hermaphroditism to dioecy. However, he knew no maphroditism via the spread of female-sterility example of it and did not consider it further. Over a mutations, phylogenetic evidence (e.g. Rieseberg century later, Charlesworth (1984) reviewed the et al., 1992; Swensen et al., 1998; Wolf et al., putative cases of androdioecy in plants and found 2001; Krahenbuhl et al., 2002; Obbard et al., 2006) none that was convincing. On the basis of her litera- and modelling (Pannell, 1997a, 2001; Wolf & ture review and evolutionary models for the evolution Takebayashi, 2004) both point to dioecy as a more and maintenance of males with hermaphrodites, likely ancestral state, with self-fertile hermaphrodites she concluded that ‘androdioecy is probably not an spreading in a population and replacing females, important phenomenon’. Since Charlesworth’s (1984) because self-fertility confers an advantage of repro- review, a number of androdioecious species have now ductive assurance in the absence of mates (Baker, been discovered amongst both plants and animals 1955; Wolf & Takebayashi, 2004). (Liston et al., 1990; Sassaman, 1991; Turner et al., It seems clear that androdioecy has evolved from 1992; Connor, 1996; Pannell, 1997b; e.g. Akimoto dioecy on several occasions, but how long can it be * e-mail: [email protected] maintained? On the one hand, we might expect Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.126, on 26 Sep 2021 at 00:44:22, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0016672307008981 J. R. Pannell 74 hermaphrodites to completely displace both females summarize the essential features that motivate the and males if selection for reproductive assurance is suf- model. These can be listed as follows: ficiently strong (Pannell, 1997a; Wolf & Takebayashi, 2004). On the other hand, androdioecy might easily 1. As noted above, although ancient in origin, revert to dioecy if selection for reproductive assurance androdioecy in Eulimnadia is derived from dioecy is relaxed, for example in response to selection for (Sassaman, 1995; Weeks et al., 2006b). Not only inbreeding avoidance or gender specialization (re- is the sister genus Metalimnadia dioecious, but viewed in Charlesworth, 1999). Certainly, both the hermaphrodites are anatomically derived from rarity of androdioecy and its generally scattered females (Zucker et al., 1997). Thus androdioecy phylogenetic distribution amongst plants and animals appears to have evolved through the displace- (Pannell, 2002; Weeks et al., 2006a) would suggest ment of females by derived hermaphrodites that that males do not tend to be maintained with her- possess an ovotestis and an ability to self-fertilize. maphrodites for long periods of evolutionary time. Hermaphrodites are also modified females in the There is, however, at least one striking exception to plants Datisca glomerata (Wolf et al., 2001) and this pattern: on the basis of a phylogenetic recon- Mercurialis annua (Pannell, 1997b). struction of the largely androdioecious crustacean 2. Eulimnadia hermaphrodites either self-fertilize their genus Eulimnadia, Weeks et al. (2006b) recently sug- progeny, or, if they are available, they outcross gested that androdioecy has been maintained for at with a male. Importantly, and unlike the situation least 24 million years and possibly for much longer. in known androdioecious plants, hermaphrodites The authors thus rejected the hypothesis that andro- cannot cross with one another (Sassaman & Weeks, dioecy ‘can only be a short-lived, transitory phase 1993). Hermaphrodites in populations that lack between hermaphroditism and dioecy (or vice versa)’ males are thus entirely self-fertilizing (Knoll & and called for a model that might ‘explain the long- Zucker, 1995; Weeks et al., 2001b), whereas her- lived coexistence of males with hermaphrodites in the maphrodites in androdioecious populations are Eulimnadia crustacean’. able to outcross by mating with males. Indeed, In this paper, I propose a model that might explain hermaphrodites show a preference for outcrossing the puzzlingly long marriage of males with hermaphro- by swimming more slowly, spending more time in dites in Eulimnadia and related androdioecious the vicinity of males and postponing self-fertiliza- species (see Longhurst, 1955; Sassaman, 1991, 1995). tion when males are absent (Medland et al., 2000; The model is in some respects similar to that of Otto Zucker et al., 2002); they thus effectively engage in et al. (1993), which predicted the frequency of males delayed self-fertilization, following opportunities in terms of male–hermaphrodite encounter and thus to outcross with males. As a result, the inbreeding outcrossing rates, inbreeding depression, effective coefficient in populations of E. texana varies sperm limitation and gender-specific viabilities for the widely, correlating negatively with the proportion species Eulimnadia texana. My model differs from of males present (Sassaman, 1989; Weeks & that of Otto et al. (1993) by incorporating details Zucker, 1999). of the natural history and genetics of androdioecy 3. Despite the high rates of selfing in some popu- in E. texana that have emerged through more recent lations, levels of inbreeding depression in E. texana research on the species. Before presenting the model, are high, with selfed progeny between 50% and I begin by briefly reviewing the empirical basis for 70% less fit than their outcrossed counterparts the new model, including details of the species’ life (Weeks et al., 1999, 2000). history and habitat, its sex-determination system, 4. Gender in Eulimnadia is determined by alleles seg- the mating behaviour of males and hermaphrodites, regating at a single locus. Males are homozygous and peculiarities concerning the expression of in- recessive, and hermaphrodites are either hetero- breeding depression. I finally discuss the implications zygous at the sex-determining locus (‘amphigenic’ of the model for the coexistence of males with hermaphrodites) or homozygous (‘monogenic’ hermaphrodites in Eulimnadia, as well as for the hermaphrodites) (Sassaman & Weeks, 1993). evolution of its sex-determining locus and the main- 5. Monogenic and amphigenic hermaphrodites are tenance of sex. morphologically and behaviourally equivalent, but the former have been found under experimen- tal conditions to be 13% less fit than the latter 2. Androdioecy in Eulimnadia (Weeks et al., 1999, 2001a); this fitness differential The natural history, phylogenetic affinities, genetics is likely to be an underestimate (see Section 4). of sex determination, mating behaviour, and variation Although sex chromosomes have not been dis- in the mating system and sex ratios of species in the cerned in Eulimnadia, it appears likely that the sex- genus Eulimnadia, especially E. texana, were recently determining locus is linked to viability loci, such reviewed by Weeks et al. (2006a). Here I briefly that the dominant hermaphrodite-determining Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.126, on 26 Sep 2021 at 00:44:22, subject to