NSFDEB-NERC: The Origin of Sperm Parasitism through the Looking Glass of the Amazon Molly

The vast majority of species have two sexes and both are needed to reproduce. But one mode of reproduction is especially interesting because it combines a seemingly impossible combination of traits. In this mode, gynogenesis, eggs have to be fertilized by males of a different species, but the genes provided by males are not incorporated into the offspring, which means that the resulting offspring are identical to their mothers. More importantly, it is often assumed that several important evolutionary changes, such as the loss of males and formation of diploid eggs, happened at the same time. Theoretically, he accumulation of large transitions in a single evolutionary step is highly unlikely, but this is nonetheless the prevailing explanation. In the proposed project, the researchers will attempt to form a synthetic gynogenetic species by carefully establishing the evolutionary and molecular pathway that led to the origin of a fish species, the Amazon molly. The research will test the assumption that major evolutionary transitions can happen simultaneously. The team located in Great Britain will be using mathematical models to guide actual experiments crossing existing species and their hybrids by a team located in the USA. This will allow a much deeper understanding of the process that leads to gynogenesis in particular and sexual reproduction in general. Furthermore, this research will provide a platform for outreach to the public via workshops and training opportunities for multiple young scientists in the STEM field.

The research aims at artificially forming a species through hybridization of two existing species determining the most likely evolutionary pathway from one to the other. The existing species at the origin of the new species are fishes from Texas and Mexico, and the new species results of a hybridization event in nature. To retrace the evolution of this species the research team will use several mathematical techniques, including differential equations and Monte-Carlo Simulations to model the most likely pathway for the evolution of a unique set of traits, including unisexuality, formation of unreduced eggs, and clonality. Current thinking claims that all of these massive changes happened in one giant evolutionary step, but this seems unlikely from a theory point of view. Guided by the mathematical models, a large-scale crossing experiment will be conducted to actually form a gynogenetic species in the laboratory. This will involve crossing sexual fishes, and also crossing the resulting F1 individuals amongst each other, and backcrossing them. Every unique cross will further be characterized genomically, genetically, and morphologically.

Gynogenesis is a highly unusual reproductive mode. In gynogenesis typically unreduced eggs develop into adults after stimulation of the egg through sperm, but without incorporation of the sperm DNA. All gynogenetic species are hybrids of two sexual species. Gynogenetic species present an evolutionary paradox: how is it possible that species experiencing the disadvantages of both sexual and asexual reproduction can outcompete sexual ancestors? Why are they not outcompeted by variants that do not depend on sperm? Here we aim to answer these questions by explaining how gynogenesis may have evolved from sexual reproduction using the Amazon molly (P. formosa) as a model organism.

The contribution of the research we propose here is twofold. On the one hand we will investigate a novel hypothesis for the evolution of gynogenesis backed by a mathematical framework. While there is abundant theoretical work showing how gynogenetic and sexual species may coexist there are no models explaining how gynogenesis originated. The prevailing hypothesis suggesting that gynogenesis is the direct outcome of hybridization stands in stark contrast with existing evidence and our preliminary results. Here we will provide the likely sequence of intermediate hybrids leading to a gynogenetic species. On the other hand, we hope to generate a gynogenetic species from two sexual ancestors. We aim to obtain not only the final product but also all the intermediate hybrids leading to the gynogenetic species. In that sense, our hypothesis will stand on genotypic and phenotypic diversity that is observed in nature.

In general, our work will contribute to understanding not only the origins of gynogenesis but also on the advantages of sexual and asexual reproduction. In particular we will develop a detailed understanding of the process of speciation of gynogenetic species.