Evolutionary History of Contagious Asexuality in Daphnia Pulex

Abstract

Abstract. Asexual taxa are short-lived, suggesting that transitions to asexuality represent evolutionary dead-ends. However, with high rates of clonal origin and coexistence of asexuals and sexuals via selective asymmetries, asexuality may persist in the long term as a result of a dynamic equilibrium between clonal origin and extinction. Few such systems have been studied in detail. Here, we investigate the evolutionary history of asexual lineages of Daphnia pulex, which are derived from sexual relatives via the inheritance of a dominant female-limited meiosis-suppressing locus and inhabit ponds throughout northeastern North America (NA). Our extensive sampling and subsequent phylogenetic analysis using mitochondrial sequence data reveals a young and genetically diverse asexual assemblage, reflecting high rates of clonal origin due to the contagious nature of asexuality. Yet, asexuality is restricted to two phylogroups (B and C) with historical and/or present associations with northeastern NA and is absent from a northwestern phylogroup (A), supporting a recent northeastern origin of asexuality in this species. Furthermore, macrogeographic patterns of genetic variability indicate that phylogroups B and C recolonized northeastern NA from opposite directions, yet their presently overlapping geographic distributions are similarly divided into an eastern asexual and a western sexual region. We attribute these patterns to a recent contagious spread of asexuality from a northeastern source. If environment-mediated selective asymmetries play no significant role in determining the outcome of competitive interactions between sexuals and asexuals, regions of contact may be setting the stage for continued asexual conquests.

What does the geography of parthenogenesis teach us about sex?

“…Alternatively, the generation of new asexual genotypes can still be ongoing, for instance via mutation [64], continuing hybridization of, or with, the sexual parents [65], contagious asexuality via endosymbiont transmission [66] or rare crossings with sexuals (e.g. [42] in hermaphrodite flatworms; [67] in Daphnia and [68] in Artemia owing to rare parthenogenetic sons), or forms of 'parasex' [69] such as horizontal gene transfer between individuals (bdelloid rotifers, see [70]) or introgression of environmental DNA (anhydrobiotic rotifers or tardigrades [71]). …”

“…Theoretically, the opposite can happen with contagious asexuality, which can make the distribution of sexual populations shrink over time (e.g. [67] in Daphnia pulex; [76]). …”

Rare diploid females coexist with rare males: a novel finding in triploid parthenogenetic populations in the psyllid Cacopsylla myrtilli (W. Wagner, 1947) (Hemiptera, Psylloidea) in northern Europe

“…This phenomenon, known as contagious parthenogenesis (Simon et al 2003), has been analyzed in detail in diploid parthenogenetic Artemia (brine shrimp) lineages (Maccari et al 2013) and in Daphnia pulex (Paland et al 2005). The formation of parthenogenesis of this type has also been experimentally demonstrated in the laboratory in Daphnia (Innes and Herbert 1988), aphids (Blackman 1972) and Artemia (Maccari et al 2014).…”

Exceptional cryptic diversity and multiple origins of parthenogenesis in a freshwater ostracod

“…In other taxa, genetically diverse asexual populations may be generated by a high rate of origin resulting in a standing diversity that is dependent, at least in part, on population size (Janko et al, 2008). High rates of origin of asexuals occur in cyclical parthenogens through repeated loss of the sexual phase, as in aphids for example (Delmotte et al, 2001;Loxdale and Lushai, 2003), and where there is repeated hybridisation, as in Poeciliopsis fish (Mateos and Vrijenhoek, 2002) or Daphnia (Paland et al, 2005). In some cases, frequent origin of asexual lineages from an ancestral sexual population clearly occurs, but the mechanism remains uncertain, as in Potamopyrgus snails (Neiman et al, 2005).…”