Population structure, mate choice, and genome transmission in naturally formed pairs in a Pelophylax lessonae–Pelophylax esculentus hybridogenetic system

Abstract

Central European water frog Pelophylax esculentus is a hybrid that lives sympatrically and forms genetic systems with one of its parental species, in this case L-E (P. lessonae - P. esculentus). Hybrids are restored in each generation due to hybridogenesis, a unique mode of hemiclonal reproduction. We investigated changes in the species composition, mate choice, and genome transmission in naturally formed pairs in the L-E hybridogenetic system from the Raków fish pond complex (SW Poland). Our observations showed that the genetic system remained the same for over a decade but the share of the taxa and the sex ratios within the species changed. The frequency of P. lessonae decreased by about 20% in favor of P. esculentus. The proportion of males to females of P. lessonae increased twofold and of P. esculentus fourfold. We also found that the stability of the L-E population was ensured by a specific female mate choice pattern with the dominance of homotypic P. lessonae and heterotypic ♀P. esculentus × ♂P. lessonae pairs (almost 90% of the pairs collected from nature). The youngest females and males that formed a successful amplexus were 3 years old. We noted a male-male competition manifested by the exclusion of young males (before the third hibernation) from the participation in the mating. An analysis of genome transmission to gametes revealed that females P. lessonae transmitted Lx, while P. esculentus transmitted the Rx and/or Lx genomes. Males of P. lessonae transmitted the Lx or Ly genomes, while P. esculentus transmitted the Lx, Ly, and/or Rx genomes. The high proportion of the L genomes transferred to gametes enables both the restoration of the parental species P. lessonae and the regular renewal of a new generation of hybrids. Significance statement Central European water frog complex includes two species: Pelophylax ridibundus (genotype RR) and P. lessonae (LL), and their natural hybrid, P. esculentus (RL). Hybrid individuals of both sexes reproduce due to a specific mode of reproduction, i.e., hybridogenesis, in which hybrids eliminate one of the parental genomes (R or L) from the germ line prior to meiosis and transmit the other one (not recombined, i.e., clonal) to the gametes. The hybrids live in mixed populations with one of the parental species and are restored in each generation. This, in turn, allows a kind of balance to be maintained in a population due to specific mate choice and genome transmission. Our research showed that the stability of the studied population was ensured by female preference to P. lessonae and male-male competition manifested by the exclusion of males under 3 years of age from the participation in the mating.

Sperm‐dependent asexual species and their role in ecology and evolution

“…Furthermore, some sperm‐dependent parthenogens do not pass on their genomes only via females, but also involve males producing unreduced or hemiclonal sperm (e.g., Pelophylax frogs [Graf & Polls‐Pelaz, 1989; Mikulíček et al, 2015; Skierska et al, 2023]) or are hermaphrodites (e.g., Schmidtea flatworms [D'Souza & Michiels, 2010], or Corbicula clams [Hedtke & Hillis, 2011; Hedtke et al, 2008]) which fertilize related sexual females, thereby also facilitating the introgression of asexual genomes back into sexual gene pools. We note that similar instances of ‘contagious asexuality’ via males are also known from some obligate parthenogens, like Daphnia water fleas (Paland et al, 2005) or Artemia crustacean (Boyer et al, 2023).…”