Plants and animals have evolved a great diversity of sexual systems that range from the extremes of obligatory self-fertilisation to complete outcrossing. Transitions between these sexual systems have long fascinated biologists due to the impacts they have on key parameters such as inbreeding depression, genetic diversity, population structure, genome structure and the evolutionary potential of species [1–7]. Transitions between sexual systems often present tradeoffs between short and long term selective advantages and can have significant connotations for the long-term viability of species. For example, selection for reproductive assurance and colonisation advantage due to mate limitation during range expansions, or as a result of high population turnover in metapopulations, can drive transitions to self-fertilisation strategies [8–10]. These transitions occur despite the deleterious effects of self-fertilisation, which include inbreeding depression, reduction in effective recombination rates and reduction in effective population size .
Transitions to androdioecy (AD) – a sexual system where males and hermaphrodites co-occur in varying frequencies in populations, with different levels of self-fertilisation and outcrossing – are extremely rare in plants and animals [12–16]. In animals, AD has only been described in five groups, rhabditid nematodes, the killifish Kryptolebias marmoratus and three crustacean groups; barnacles, a genus of clam shrimps Eulimnadia, and in the order Notostraca, the tadpole shrimps [17, 18]. AD can evolve either through the invasion of males into hermaphrodite only populations, as in barnacles [18, 19], or through the replacement of females with hermaphrodites in gonochoric populations (where males and females are found in approximate equality), as in the plants Mercurialis annua[20, 21] and Datisca glomerata. As models to describe the evolution and maintenance of AD only predict its evolution under stringent conditions, AD has historically been considered an unstable, transitional sexual system between gonochorism and hermaphroditism (or vice versa) [12–14, 23, 24]. This view is borne out by the scarcity of AD in nature [12, 17], although recent research in the branchiopod Eulimnadia has revealed an unexpected stability of androdioecy .
Notostraca, or tadpole shrimps, is a small order of branchiopod crustaceans characterised by a high level of morphological stasis. Fossils dating back as far as the Triassic are almost indistinguishable from contemporary species leading them to be referred to as ‘living fossils’ [26–30]. In contrast, Notostraca has diverse sexual systems, including gonochorism, self-fertile hermaphroditism and AD, with variation occurring on both an interspecific and intraspecific level [31, 32]. Remarkably, AD is found in species from both notostracan genera, Triops and Lepidurus, suggesting that transitions in reproductive system might have evolved repeatedly in the order. Despite this, the evolutionary history of reproductive systems in Notostraca is unknown due to the lack of a resolved phylogeny [33, 34], and the poor knowledge of the diversity of the group, partly due to the widespread presence of cryptic species [32, 35–38]. Gonochorism has been hypothesized to be the ancestral state in the group, and the evolution of self-fertile hermaphroditism and AD has been linked to reproductive assurance in the context of range expansions, possibly after glacial retreat [8, 31, 39, 40], although this has never been explicitly tested.
Here we combine newly generated and GenBank sequence data to assess Notostraca taxonomic diversity, identifying considerable cryptic diversity, and employ a multigene phylogenetic approach to create a well-supported, global phylogeny of Notostraca. Information on sexual system was compiled and Maximum Parsimony (MP) and model-based Maximum Likelihood (ML) character mapping approaches were used on the phylogeny to investigate sexual system evolution across the order. We also tested the hypothesis that reproductive assurance has driven the evolution of self-fertilisation across Notostraca [8, 39]. Taxa found at higher latitudes are likely to have experienced bouts of colonisation during post glacial range expansions, which would select for AD/hermaphroditism. We therefore compared the latitudes that AD/hermaphroditic and gonochoric taxa are found using a phylogenetic t-test. Our analyses reveal high levels of reproductive lability with frequent transitions occurring to and from androdioecy. Furthermore, this flexibility is conserved across Notostraca, and may have been maintained for at least 250 million years. Additionally, AD/hermaphroditic taxa are found at significantly higher latitudes than gonochoric ones suggesting that colonisation advantage through reproductive assurance is likely to be involved in transitions between sexual systems in Notostraca.