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Comparative studies of inbreeding effects on evolutionary processes in non-model animal populations

Final Report Summary - ECOGENOMICINBREEDING (Comparative studies of inbreeding effects on evolutionary processes in non-model animal populations)

Across several animal taxa, the evolution of sociality and group living involves a suite of characteristics, a so-called “social syndrome,” that includes cooperative breeding, reproductive bias which means that only a few females in a group reproduce, primary female-biased sex ratio – the production of more females than males, and the transition from outcrossing to inbreeding mating system. These factors contribute to processes that result in loss of genetic diversity and a reduction in effective population size, which is a measure of the number of individuals in a population that contribute offspring to the next generation. This is an extremely important factor for maintaining population genetic diversity and thereby for the potential of a population to persist and adapt to environmental change. So while the social syndrome may be favoured by short-term benefits, for example easy access to mates, it may come with long term costs, because the reduction in effective population size amplifies loss of genetic diversity, and ultimately restricts the potential of populations to respond to environmental change. In this project, we investigated the consequences of the social syndrome on genetic diversity using social spiders of the genus Stegodyphus as study system. By comparative DNA sequencing, the genomes of several social spider species was investigated to estimate genome-wide diversity in spider species that differed in level of sociality, reproductive skew and mating system. We found that genetic diversity was up to 10 times lower in social compared to solitary and outbreeding species, and an associated tenfold reduction in effective population size of social populations. These results suggest that animal species with this social syndrome experience severe loss of genome-wide diversity, which is likely to limit their ability to persist as species over evolutionary time scales. The social syndrome therefore increases the risk of extinction.

Social spiders also consistently show female biased sex ratio, which is expected to incur benefits in terms of productivity for the group. We investigated the mechanisms behind the production of more females than males, by quantifying the production of male and female determining sperm cells using a sophisticated cell counting technique. We show that males of social species produce a higher proportion of female-determining sperm than male-determining sperm, which is consistent with the production of more daughters. This new result suggests that the sex that carries only one copy of the sex chromosomes, here males, is more likely to evolve control of sex ratio of the offspring. We also investigated whether bacterial symbionts, which are microorganisms within the spider, may explain the over-production of females. This was done by sequencing of microbes that are known to be able to affect the sex of their hosts’ offspring. We found that the five common types of bacterial symbionts that are known to affect offspring sex ratio are largely absent, showing that these bacteria are not responsible for the biased sex ratio in social spiders.

In this project, we also sequenced and assembled the first spider genomes, which provides an important source for developing new and comparative research opportunities. We then studied the genetic basis of spider and insect immune systems, and demonstrated how spiders have evolved differently from other arthropods. We have also characterized proteins that are important for the adaptation of spiders to local conditions. With this broad scientific research programme, this project has established social spiders as an important model system in research on the evolutionary biology of life history and mating systems.