Hybridization and the Origin of Contagious Asexuality inDaphnia pulex

Abstract

Hybridization plays a potentially important role in the origin of obligate parthenogenesis (OP) in many organisms. However, it remains controversial whether hybridization directly triggers the transition from sexual reproduction to obligate asexuality or a hybrid genetic background enables asexual species to persist. Furthermore, we know little about the specific genetic elements from the divergent, yet still hybridizing lineages responsible for this transition and how these elements are further spread to create other OP lineages. In this study, we address these questions in Daphnia pulex, where cyclically parthenogenetic (CP) and OP lineages coexist. Ancestry estimates and whole-genome association mapping using 32 OP isolates suggest that a complex hybridization history between the parental species D. pulex and D. pulicaria is responsible for the introgression of a set of 647 D. pulicaria single nucleotide polymorphism alleles that show perfect association with OP. Crossing experiments using males of OP lineages and females of CP lineages strongly support a polygenic basis for OP. Single-sperm analyses show that although normal meiotic recombination occurs in the production of haploid sperm by males of OP lineages, a significant proportion of such sperm are polyploid, suggesting that the spread of asexual elements through these males (i.e., contagious asexuality) is much less efficient than previously envisioned. Although the current Daphnia genome annotation does not provide mechanistic insight into the nature of the asexuality-associated alleles, these alleles should be considered as candidates for future investigations on the genetic underpinnings of OP.

Insertion polymorphisms of mobile genetic elements in sexual and asexual populations of Daphnia pulex

“…(2012) is confirmed in all the 10 isolates from Tucker et al (2013) by this algorithm, demonstrating that our pipeline can efficiently identify TE insertion sites if the relevant TE sequences are included in the TE library. Interestingly, we also identified additional 5 insertion sites of this TE sequence in asexual isolates but absent in all 20 sexual isolates, among which 2 and 3 are identified in all the 10 isolates from Tucker et al (2013) and Xu et al (2015), respectively. However, there is no fixed asexual-specific insertion of this TE sequence.…”

“…This is likely the reason why the TE insertion found by Eads et al. (2012) was not identified in the isolates from Xu et al. (2015) and why this TE sequence is distributed in normal and urban isolates at distinct locations.…”

“…A principle component analysis using SNPs characterized in the latter study showed that the normal and “urban” asexual D. pulex isolates are clustered separately (see fig. 1 in Xu et al. 2015).…”

“…In this study, we used 20 asexual D. pulex isolates from two different sources: 10 normal isolates from Tucker et al (2013) and 10 “urban” isolates from Xu et al (2015). A principle component analysis using SNPs characterized in the latter study showed that the normal and “urban” asexual D. pulex isolates are clustered separately (see fig.…”

“…In contrast, asexual D. pulex lineages lose the ability to engage in sexual reproduction and reproduce strictly by obligate parthenogenesis in any environment. Interestingly, the lack of sexual reproduction in asexual lineages is limited to females, and males produced by some asexual females are still capable of haploid gamete production, providing a way for transferring asexuality elements to sexual populations via backcrossing (Innes and Hebert 1988; Xu et al. 2015).…”