High lability of sexual system over 250 million years of evolution in morphologically conservative tadpole shrimps

Abstract

BackgroundSexual system is a key factor affecting the genetic diversity, population structure, genome structure and the evolutionary potential of species. The sexual system androdioecy – where males and hermaphrodites coexist in populations – is extremely rare, yet is found in three crustacean groups, barnacles, a genus of clam shrimps Eulimnadia, and in the order Notostraca, the tadpole shrimps. In the ancient crustacean order Notostraca, high morphological conservatism contrasts with a wide diversity of sexual systems, including androdioecy. An understanding of the evolution of sexual systems in this group has been hampered by poor phylogenetic resolution and confounded by the widespread occurrence of cryptic species. Here we use a multigene supermatrix for 30 taxa to produce a comprehensive phylogenetic reconstruction of Notostraca. Based on this phylogenetic reconstruction we use character mapping techniques to investigate the evolution of sexual systems. We also tested the hypothesis that reproductive assurance has driven the evolution of androdioecy in Notostraca.ResultsCharacter mapping analysis showed that sexual system is an extremely flexible trait within Notostraca, with repeated shifts between gonochorism and androdioecy, the latter having evolved a minimum of five times. In agreement with the reproductive assurance hypothesis androdioecious notostracans are found at significantly higher latitudes than gonochoric ones indicating that post glacial re-colonisation may have selected for the higher colonisation ability conferred by androdioecy.ConclusionsIn contrast to their conserved morphology, sexual system in Notostraca is highly labile and the rare reproductive mode androdioecy has evolved repeatedly within the order. Furthermore, we conclude that this lability of sexual system has been maintained for at least 250 million years and may have contributed to the long term evolutionary persistence of Notostraca. Our results further our understanding of the evolution of androdioecy and indicate that reproductive assurance is a recurrent theme involved in the evolution of this sexual system.

Molecular phylogeny of the Notostraca

“…Trusheim's (1938) interpretation that the morphology of the Triassic T. cancriformis minor resembled that of extant Triops (see above) thus appears plausible, which supports its present position within the genus Triops. Mathers et al (2013b) recently suggested a minimum age of 250 Ma BP for the initial diversification into Triops and Lepidurus. This date comes close to our age estimate of 152.3-233.5 Ma BP (node 2 in Table 3).…”

“…The lineage comprising the American endemics L. lemmoni, L. bilobatus and almost certainly also L. packardi and L. cryptus (see Fig. 1a in Mathers et al, 2013b) could have dispersed from Europe westwards to Northern America via the Thulean Bridge (see Fig. S.4), which is thought to have been an important route for faunal exchange in the Early Eocene, at approx.…”

“…They also included no more than two DNA markers to infer phylogenies, resulting in poor resolution especially of within-genus topologies (e.g. Vanschoenwinkel et al, 2012;Mantovani et al, 2004; but see Mantovani et al, 2009;Mathers et al, 2013b, for well resolved topologies, the latter two with a combined analysis of three, and seven markers, respectively). Moreover, until recently (see Mathers et al, 2013b), it remained unclear if both extant genera, Triops and Lepidurus, were monophyletic (e.g.…”

“…Vanschoenwinkel et al, 2012;Mantovani et al, 2004; but see Mantovani et al, 2009;Mathers et al, 2013b, for well resolved topologies, the latter two with a combined analysis of three, and seven markers, respectively). Moreover, until recently (see Mathers et al, 2013b), it remained unclear if both extant genera, Triops and Lepidurus, were monophyletic (e.g. Vanschoenwinkel et al, 2012;Mantovani et al, 2004).…”

“…Vanschoenwinkel et al, 2012;Mantovani et al, 2004). The most recent estimates for the date of initial divergence into the two genera span an extensive range, from 12.75 to at least 250 Ma BP (Vanschoenwinkel et al, 2012;Mathers et al, 2013b). First attempts to obtain DNA-based estimates for this split (Vanschoenwinkel et al, 2012) and for divergences among lineages within the genera relied on 'molecular clocks' derived from non-branchiopod taxa Vanschoenwinkel et al, 2012).…”