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Final Report Summary - DAMANMP (Evolution of partly genetic sex determination in Daphnia)

In the animal kingdom, sex determination occurs along a continuum between genetic sex determination (GSD) and environmental sex determination (ESD). Under GSD, sex is determined genetically, meaning that males and females have different alleles or genotypes at one or several loci. Under ESD, any genotype can develop into a male or a female, depending on environmental cues. ESD is thought to be ancestral in animals and the evolutionary transition from ESD to GSD is believed to be closely linked with the initial steps of sex-chromosome evolution. However, due to a lack of suitable empirical systems, the early stages of this transition remain poorly understood.
In the small freshwater crustacean Daphnia, parthenogenetic reproduction alternates with sexual reproduction. Individuals of both sexes that belong to the same parthenogenetic line are genetically identical and their sex is determined by the environment. However, some Daphnia never produce males, and these non male producing ("NMP") genotypes can only persist through phases of sexual reproduction if they co-occur with normal ("MP") genotypes that have ESD and, depending on the environment, produce either males or females. The distinction between MP and NMP is heritable, NMP being dominant in heterozygous genotypes. Hence, Daphnia have a partially genetic and partially environmental sex determination. Here I exploit this unique polymorphism to study the early stages of the evolutionary transition between ESD and GSD and to investigate its genetic basis and genetic/genomic consequences, including the evolution of novel sex chromosomes.
Progress and results on the three objectives:
Objective1. The genetic basis and evolutionary origin of NMP (largely completed): NMP is determined by a genomic region showing characteristics of a young W sex-chromosome and containing several genes known to be involved in sex determination in arthropods. Recombination suppression in this region appears to be ancestral, suggesting that pre-existing regions with low recombination may play an underappreciated role in the early evolution of sex chromosomes. Finally, a gene expression study shows that NMP is a tightly regulated phenotype, suggesting secondary evolutionary integration of the initial sex-determining mutation, in agreement with sex-chromosome evolution theory.
Objective2. The evolutionary advantage of NMP (data collection mostly completed, data analysis ongoing): We provide evidence for two evolutionary advantages of NMP: Obligate outcrossing and avoidance of plasticity costs. Both costs may be important also in other ESD-GSD transitions. We quantified both costs to predict and test equilibrium frequencies of NMP.
Objective3. Male specialization in MP (only partly completed due to deviations from the original plans, fall-back strategies initiated): Despite the failure of an experimental evolution study, we were able to demonstrate that male specialization in MP occurs in nature, and to obtain a quantitative estimate of the degree of this specialization.
Overall, the results establish the NMP/MP polymorphism in Daphnia as a major animal systems for studying the initial stages of sex-chromosome evolution and the evolutionary transition from ESD to GSD. The primary impact is thus scientific. Furthermore, in accordance with the CIG call, the project has strongly advanced the careers of the fellow and all other personnel involved.

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Life Sciences
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