Evolution of Self-fertilization in Hermaphrodites : an Animal Perspective – ESHAP

Our project faces three technical challenges. The first is to explore the diversity of selfing rates in a hitherto understudied group. Molecular biology techniques provide estimates of selfing rates from samples of natural populations, but till recently used to require a large investment for each new species studied. We used next generation sequencing methods (dd-RADseq) to develop a protocol allowing the study of arbitrary numbers of new species without specific technical developments for each.
A second challenge is that plants, the classical model system for the study of mating system evolution, have too long generation times to observe evolution directly. With our short-generation animal model (2 months) we have been able to test theoretical models using experimental evolution over tens of generations. Finally, we were able to compare the demographic performances associated with both reproductive modes, using a long-term field survey (15 yr) on two closely related species, one selfing the other outcrossing.

We detected the initiation of an evolutionary transition towards selfing in the laboratory : in twenty generations snail adopted traits favoring self-fertilization under conditions of reduced mate availability. In addition, selfing became less costly, owing to the elimination of some deleterious mutations initially present in genomes. These results support a scenario that had been often formulated, but never observed.
In addition, selfing populations initially respond to selection more rapidly, but this response rapidly stops, confirming the theoretical expectation of a negative effect of selfing on the evolutionary potential of populations.

This project brings basic knowledge on the evolution of hermaphroditism, mating systems and sex allocation. In addition, it increases our knowledge on particular species of applied interest : Lymnaea stagnalis (a sentinel species in freshwater ecotoxicology) , Biomphalaria glabrata and Lymnaea columella (vectors of human and cattle parasites).

Eight scientific papers have come out of this project to date, all in english in international high-impact journals. The highest-impact publication is certainly a paper in Current Biology where we experimentally validate, for the first time, the long-held hypothesis of selfing as an evolutionary « dead-end » with reduced evolutionary potential. We also communicated our results to the general public and high-school classes through conferences, and through a short TV program in the M6 channel.

In this project we will study how self-fertilization evolves and its evolutionary consequences in hermaphroditic animals . A strong limitation of the theory of mating system evolution is that it has been tested quasi exclusively in flowering plants. This poses problems of generality (to what extent do the arguments made depend on specificities of this group ?) and feasibility (most plants are not easily amenable to multi-generation experiments such as experimental evolution). For these two reasons it is urgent to develop animal models. We will here focus on a group of freshwater snails (basommatophorans) with highly diverse mating systems, presenting a suite of advantages making them ideal to address hitherto unsolved questions.
We will focus on evolutionary transitions between outcrossing and selfing, how and when they occur, and their consequences. In particular we will test the long-standing hypothesis that selfing is an evolutionary dead-end in two ways. First we will characterize the number and unidirectionality of transitions in the phylogeny; second, we will empirically test the key steps of the most plausible scenario describing how an outcrossing species can become a preferential selfer (but not the reverse). The main components of this scenario are (i) constraints on mate or pollen availability resulting in a selection for selfing as a reproductive insurance. (ii) the existence of an intermediate state of preferential outcrossing with delayed, optional selfng when mates are lacking. (iii) the purging of inbreeding depression, resulting in runaway selection for selfing and even less inbreeding depression. (iv) the lack of adaptive potential in selfers, resulting in high extinction rates. All these aspects will be tested experimentally by looking at experimental evolution under elevated contraints on mating (frequent lack of mates), by measuring response to artificial and natural selection in pairs of outcrossing/selfing species living in the same environment, and by comparing their ability to colonize empty sites, estimated from metapopulation studies in the field
This project is very ambitious in terms of (i) gathering molecular polymorphism data from many hitherto unstudied species, (ii) the number of size of experiments, and (iii) the requirement for long-term field data. It brings together a highly qualified consortium with previous experience of common work and complementary skills. Among the expected breakthroughs of this project will be the first experimental-evolution study of mating system evolution; and the first unbiased estimates of the frequency of mixed-mating in animals, and why it seems to be lower than in plants. All this will serve our ambition to establish animals, and especially basommatophoran snails, as essential models for mating system theory.