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The evolutionary consequences of inbreeding in natural populations: Genotypic-phenotypic interactions and implications for genetic diversity and evolutionary potential

Final Report Summary - ECOGENOMICS (The evolutionary consequences of inbreeding in natural populations: Genotypic-phenotypic interactions and implications for genetic diversity …)

The aim of this project is to study the evolutionary consequences of inbreeding for genetic diversity and evolutionary potential in natural populations of social spiders. Social spiders constitute a particularly suitable model system for studying the evolutionary consequences of inbreeding, because they exhibit varying levels of inbreeding and social organisation: the genus Stegodyphus, which is the study system of this project, contains three independently evolved social and inbreeding species and 15 solitary and outbreeding species. This system allows for comparative studies by contrasting genetic, genomic and life history parameters of inbreeding and outbreeding species.

The transition from outbreeding solitary to inbreeding social living may pose a dilemma, since inbreeding is often associated with the expression of deleterious recessive alleles. Furthermore, increased homozygosity and female biased sex ratio in social inbreeding species can lead to relaxed selection and a build-up of deleterious mutations, which in the long run may cause a decline in the ability to adapt to environmental change.

The overall aim of the study is to quantify the potential two-fold cost of inbreeding, short-term and long-term effects combining empirical research and state-of-the-art genomic tools.

Objectives and progress:

1) Short-term potential cost of increased homozygosity is investigated experimentally in natural populations of social Stegodyphus spiders, in an experimental design where reproductive success and offspring performance was compared among inbred and outbred crosses. Adult spiders are crossed (either inbreeding or outbreeding) and their reproductive success is being recorded.
2) To determine population genetic structure and estimate patterns of gene flow we applied AFLP markers (genetic fingerprinting) to assess gene flow mediated by male and female dispersal in natural populations. Our data suggest that social spider colonies are founded by mated females and there is very limited male mediated gene flow. This leads to highly structured populations, and mating among related colony members lead to even higher degree of inbreeding.
3) Long-term consequences of inbreeding may be revealed in loss of genetic variation and reduced evolutionary potential. To test the evolutionary hypothesis that the transition to sociality and inbreeding is associated with loss of genetic diversity, I am using next-generation sequencing to identify coding regions and develop SNPs to compare genetic variation in inbreeding and outbreeding clades of the genus Stegodyphus. So far I have sequenced the transcriptomes of three Stegodyphus species which will be compared to identify genes that are conserved across species. I will then use a set of common genes to sequence inbreeding and outbreeding species to estimate genetic variation and molecular evolution.

In addition, I will build a molecular phylogeny which serves as a backbone for comparative studies and verifies the hypothesised evolutionary transitions from outbreeding solitary to inbreeding social systems.

The research is progressing very well, and it is expected that data will be collected to test the hypothesis that regular inbreeding may lead to reduced genetic variation within populations and may reduce the potential for adaptation.

The research furthermore opens interesting avenues for future projects, and the researcher is preparing a European Research Council (ERC) starting grant application based on the technologies and research platform generated within this grant period.