Periodic Reporting for period 1 - IsoBar (Relative Role of Reproductive Isolating Barriers During Speciation)
Reporting period: 2016-03-11 to 2018-03-10
The overall research objective of this project is to understand the relative importance of different isolating barriers during adaptive speciation. The project is focused on pea aphids, Acyrthosiphon pisum, which feed on legumes and form multiple host races, each adapted to one or few legume plants. Two reproductive isolation barriers separate the host races: habitat choice (encounters and mating among races is minimal due to strong host preference) and post-zygotic isolation (hybrids among races have low fecundity on paternal host plants).
This project investigates the evolution of reproductive isolation which is central to the origin and maintenance of biodiversity. It also provided a more complete understanding of the evolutionary history of pea aphids, which represent one of the pest species of highest agricultural importance in temperate regions.
This project investigates the evolution of reproductive isolation which is central to the origin and maintenance of biodiversity. It also provided a more complete understanding of the evolutionary history of pea aphids, which represent one of the pest species of highest agricultural importance in temperate regions.
We tested if distantly related pea aphid host races have additional prezygotic isolation barriers compared to more closely related ones. We observed mating behaviour and egg fertilization rates for three types of crosses: among individuals of the same host race, between closely related host races, and between distantly related host races. We did not find significant differences in mating behaviour among three types of crosses, but we observed drastic reduction in the number of fertilized eggs for the crosses between distantly related host races. From this we infer the presence of post-mating pre-zygotic barrier in the more distantly related host races.
We generated and analysed whole-genome sequencing data (61 genomes at 20x coverage) to infer patterns associated with different reproductive isolation barriers. Results of genome-wide sliding window analysis show that for the closely related host races – separated by habitat choice and post-zygotic isolation – genomic divergence is variable, but overall relatively weak. For the distantly related host races – in addition isolated by the pre-zygotic post-mating barrier – genomic divergence is variable but overall stronger. We also find that sex chromosome divergence for the distantly related host races is higher and less variable than autosomal. Using cytogenetic approaches, we confirmed that higher sex chromosome divergence is not related to unstable karyotypes (i.e. different chromosome number) in distantly related host races.
We estimated gene flow for distantly and closely related host races, based on neutral sites across the genome, using a diffusion approximation. Our results show that gene flow is very limited between distantly related host-races compared with closely related ones (about 5 times smaller). This suggests an important role of the intrinsic pre-zygotic isolation barrier at impeding gene flow.
We also investigated accumulation of genomic divergence in a model of ecological speciation with gene flow. Our results show that at early stages of speciation, divergence is limited to the loci under selection. At a later stage of speciation, neutral loci also become differentiated. In the parameter space we examined, we did not find homogeneous widespread divergence across the genome. This may be explained by episodes of gene flow diminishing divergence at neutral loci. However, it turned out that the model of speciation with gene flow is not suitable for the pea aphid system. During implementation of this project, we re-examined the age of the pea aphid radiation by estimating genome-wide divergence (using sequencing data from this project) and by estimating spontaneous mutation rate for pea aphids. Our results show that pea aphids diversified about 500 thousand years ago (contrary to previous estimates of about 10 thousand years ago). This ancient pea aphid radiation suggests host race formation may have been influenced by geographic isolation during Pleistocene climatic oscillations.
Overall, our results suggest that completion of speciation in the pea aphid complex is largely affected by intrinsic post-mating pre-zygotic reproductive isolation. It is accompanied by strong genomic divergence, especially on the sex chromosome. Genomic patterns of divergence cannot be interpreted under scenario of speciation with gene flow due to the age and possible contribution of allopatric isolation to diversification of the pea aphids.
Results of this project were reported at five international research conferences and three research papers (1 published, 2 in preparation). Knowledge transfer has also occurred at daily interactions, group meetings and journal clubs. Results of the project were (and the remaining results will also be) published with open access via the green route. Two public dissemination events were carried out.
The researcher enhanced career perspectives by receiving training in the fields of population genomics and experimental biology, by developing own network of collaborations, and by obtaining project management experience.
We generated and analysed whole-genome sequencing data (61 genomes at 20x coverage) to infer patterns associated with different reproductive isolation barriers. Results of genome-wide sliding window analysis show that for the closely related host races – separated by habitat choice and post-zygotic isolation – genomic divergence is variable, but overall relatively weak. For the distantly related host races – in addition isolated by the pre-zygotic post-mating barrier – genomic divergence is variable but overall stronger. We also find that sex chromosome divergence for the distantly related host races is higher and less variable than autosomal. Using cytogenetic approaches, we confirmed that higher sex chromosome divergence is not related to unstable karyotypes (i.e. different chromosome number) in distantly related host races.
We estimated gene flow for distantly and closely related host races, based on neutral sites across the genome, using a diffusion approximation. Our results show that gene flow is very limited between distantly related host-races compared with closely related ones (about 5 times smaller). This suggests an important role of the intrinsic pre-zygotic isolation barrier at impeding gene flow.
We also investigated accumulation of genomic divergence in a model of ecological speciation with gene flow. Our results show that at early stages of speciation, divergence is limited to the loci under selection. At a later stage of speciation, neutral loci also become differentiated. In the parameter space we examined, we did not find homogeneous widespread divergence across the genome. This may be explained by episodes of gene flow diminishing divergence at neutral loci. However, it turned out that the model of speciation with gene flow is not suitable for the pea aphid system. During implementation of this project, we re-examined the age of the pea aphid radiation by estimating genome-wide divergence (using sequencing data from this project) and by estimating spontaneous mutation rate for pea aphids. Our results show that pea aphids diversified about 500 thousand years ago (contrary to previous estimates of about 10 thousand years ago). This ancient pea aphid radiation suggests host race formation may have been influenced by geographic isolation during Pleistocene climatic oscillations.
Overall, our results suggest that completion of speciation in the pea aphid complex is largely affected by intrinsic post-mating pre-zygotic reproductive isolation. It is accompanied by strong genomic divergence, especially on the sex chromosome. Genomic patterns of divergence cannot be interpreted under scenario of speciation with gene flow due to the age and possible contribution of allopatric isolation to diversification of the pea aphids.
Results of this project were reported at five international research conferences and three research papers (1 published, 2 in preparation). Knowledge transfer has also occurred at daily interactions, group meetings and journal clubs. Results of the project were (and the remaining results will also be) published with open access via the green route. Two public dissemination events were carried out.
The researcher enhanced career perspectives by receiving training in the fields of population genomics and experimental biology, by developing own network of collaborations, and by obtaining project management experience.
This project made several contributions beyond the state of the art:
i) clarification of evolutionary history of pea aphids, by performing first phylogenomic reconstruction and by re-examining the age of radiation;
ii) identification of novel reproductive barrier in the pea aphids – intrinsic post-mating pre-zygotic isolation, which is very strong and acts at the late speciation stages;
iii) provision of first estimate of spontaneous mutation rate during parthenogenetic generations for aphids;
iv) development of numerical modelling approaches for investigating build-up of genomic divergence during speciation.
Main socio-economic impact of this project will most likely come from the results on estimation of the age of the pea aphid radiation, as our results rule out effect of early human agriculture on their diversification.
i) clarification of evolutionary history of pea aphids, by performing first phylogenomic reconstruction and by re-examining the age of radiation;
ii) identification of novel reproductive barrier in the pea aphids – intrinsic post-mating pre-zygotic isolation, which is very strong and acts at the late speciation stages;
iii) provision of first estimate of spontaneous mutation rate during parthenogenetic generations for aphids;
iv) development of numerical modelling approaches for investigating build-up of genomic divergence during speciation.
Main socio-economic impact of this project will most likely come from the results on estimation of the age of the pea aphid radiation, as our results rule out effect of early human agriculture on their diversification.