The role of hybridization in the origin and spread of asexuality in Daphnia

Abstract

The molecular mechanisms leading to asexuality remain little understood despite their substantial bearing on why sexual reproduction is dominant in nature. Here, we examine the role of hybridization in the origin and spread of obligate asexuality in Daphnia pulex, arguably the best-documented case of contagious asexuality. Obligately parthenogenetic (OP) clones of D. pulex have traditionally been separated into 'hybrid' (Ldh SF) and 'nonhybrid' (Ldh SS) forms because the lactase dehydrogenase (Ldh) locus distinguishes the cyclically parthenogenetic (CP) lake dwelling Daphnia pulicaria (Ldh FF) from its ephemeral pond dwelling sister species D. pulex (Ldh SS). The results of our population genetic analyses based on microsatellite loci suggest that both Ldh SS and SF OP individuals can originate from the crossing of CP female F1 (D. pulex × D. pulicaria) and backcross with males from OP lineages carrying genes that suppress meiosis specifically in female offspring. In previous studies, a suite of diagnostic markers was found to be associated with OP in Ldh SS D. pulex lineages. Our association mapping supports a similar genetic mechanism for the spread of obligate parthenogenesis in Ldh SF OP individuals. Interestingly, our study shows that CP D. pulicaria carry many of the diagnostic microsatellite alleles associated with obligate parthenogenesis. We argue that the assemblage of mutations that suppress meiosis and underlie obligate parthenogenesis in D. pulex originated due to a unique historical hybridization and introgression event between D. pulex and D. pulicaria.

Keywords: Daphnia pulex; Daphnia pulicaria; asexuality; hybridization; meiosis suppression; parthenogenesis.

Figure 1

The transmission of meiosis suppression in Daphnia pulex. (A) The Ldh SF and SS obligately parthenogenetic (OP) D. pulex hybrids can originate from backcrossing between F₁ cyclically parthenogenetic (CP) hybrids of Daphnia pulex (white) × Daphnia pulicaria (grey) with D. pulex males carrying meiosis-suppression genes. Stars indicate obligately parthenogenetic individuals. (B) Females of pure D. pulex can mate with Ldh SS OP males with some D. pulicaria genes, giving rise to both CP and OP offspring with some D. pulicaria genes (grey).

Figure 2

Neighbor-joining (NJ) tree (A) and Bayesian estimates of ancestry (B) for cyclically parthenogenetic Daphnia pulex, Daphnia pulicaria, and obligately parthenogenetic D. pulex individuals based on nine microsatellite markers. Dashed lines in the NJ tree designate obligate parthenogens (OP, both Ldh SS and SF), with the black circles designating Ldh SS OP individuals, whereas grey lines and black lines represent cyclically parthenogenetic D. pulicaria and D. pulex individuals, respectively. Each vertical bar of the Bayesian estimates of ancestry represents a genotype, with the black and grey colour representing the probability that an individual is derived from a D. pulex and D. pulicaria genetic background, respectively (ordered by increasing probability of D. pulicaria). Ldh SF hybrid OP and Ldh SS OP represent lineages in the hybrid clade (panel A), whereas Ldh SS D. pulex OP are lineages from the D. pulex clade (panel A).

Figure 3

Hybrid index for A) Ldh SS OP, B) Ldh SF OP, C) simulated backcrosses between F₁ and Daphnia pulex, and D) simulated F₁. Samples were analyzed with the Introgress program (Gompert & Buerkle 2009, 2010) using the D. pulex (H index = 0.0) and Daphnia pulicaria (H index = 1.0) nine microsatellite loci as the reference parental genotypes.