Low Spontaneous Mutation Rate and Pleistocene Radiation of Pea Aphids.

Accurate estimates of divergence times are essential to understand the evolutionary history of species. It allows linking evolutionary histories of the diverging lineages with past geological, climatic, and other changes in environment and shed light on the processes involved in speciation. The pea aphid radiation includes multiple host races adapted to different legume host plants. It is thought that diversification in this system occurred very recently, over the past 8,000-16,000 years. This young age estimate was used to link diversification in pea aphids to the onset of human agriculture, and led to the establishment of the pea aphid radiation as a model system in the study of speciation with gene flow. Here, we re-examine the age of the pea aphid radiation, by combining a mutation accumulation experiment with a genome-wide estimate of divergence between distantly related pea aphid host races. We estimate the spontaneous mutation rate for pea aphids as 2.7×10-10 per haploid genome per parthenogenic generation. Using this estimate of mutation rate and the genome-wide genetic differentiation observed between pea aphid host races, we show that the pea aphid radiation is much more ancient than assumed previously, predating Neolithic agriculture by several hundreds of thousands of years. Our results rule out human agriculture as the driver of diversification of the pea aphid radiation, and call for re-assessment of the role of allopatric isolation during Pleistocene climatic oscillations in divergence of the pea aphid complex.

Intrinsic pre-zygotic reproductive isolation of distantly related pea aphid host races.

Human activities may weaken or destroy reproductive isolation between young taxa, leading to their fusion with consequences for population and community ecology. Pea aphid host races are adapted to different legume taxa, providing a degree of pre-mating isolation mediated by habitat choice. Yet, all races can feed and reproduce on the broad bean (Vicia faba), a major crop which represents a 'universal host plant', which can promote hybridization between races. Here, we ask if pea aphid host races have reproductive barriers which prevent or reduce gene flow when they co-occur on the universal host plant. We observed mating behaviour, female survival, number of eggs 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 and female survival among the three types of crosses. However, we observed a drastic reduction in the number of eggs laid, and in the number of fertilized eggs, in distant crosses. We conclude that widespread broad bean cultivation in agriculture may predispose closely related-but not distantly related-host races to hybridize, disrupting reproductive isolation between incipient species.

Repeated unidirectional introgression of nuclear and mitochondrial DNA between four congeneric Tanganyikan cichlids.

With an increasing number of reported cases of hybridization and introgression, interspecific gene flow between animals has recently become a widely accepted and broadly studied phenomenon. In this study, we examine patterns of hybridization and introgression in Ophthalmotilapia spp., a genus of cichlid fish from Lake Tanganyika, using mitochondrial and nuclear DNA from all four species in the genus and including specimens from over 800 km of shoreline. These four species have very different, partially overlapping distribution ranges, thus allowing us to study in detail patterns of gene flow between sympatric and allopatric populations of the different species. We show that a significant proportion of individuals of the lake-wide distributed O. nasuta carry mitochondrial and/or nuclear DNA typical of other Ophthalmotilapia species. Strikingly, all such individuals were found in populations living in sympatry with each of the other Ophthalmotilapia species, strongly suggesting that this pattern originated by repeated and independent episodes of genetic exchange in different parts of the lake, with unidirectional introgression occurring into O. nasuta. Our analysis rejects the hypotheses that unidirectional introgression is caused by natural selection favoring heterospecific DNA, by skewed abundances of Ophthalmotilapia species or by hybridization events occurring during a putative spatial expansion in O. nasuta. Instead, cytonuclear incompatibilities or asymmetric behavioral reproductive isolation seem to have driven repeated, unidirectional introgression of nuclear and mitochondrial DNA into O. nasuta in different parts of the lake.

When environmental changes do not cause geographic separation of fauna: differential responses of Baikalian invertebrates.

BACKGROUND: While the impact of climate fluctuations on the demographic histories of species caused by changes in habitat availability is well studied, populations of species from systems without geographic isolation have received comparatively little attention. Using CO1 mitochondrial sequences, we analysed phylogeographic patterns and demographic histories of populations of five species (four gastropod and one amphipod species) co-occurring in the southwestern shore of Lake Baikal, an area where environmental oscillations have not resulted in geographical isolation of habitats. RESULTS: Species with stronger habitat preferences (gastropods B. turriformis, B. carinata and B. carinatocostata) exhibit rather stable population sizes through their evolutionary history, and their phylogeographic pattern indicates moderate habitat fragmentation. Conversely, species without strong habitat preference (gastropod M. herderiana and amphipod G. fasciatus) exhibit haplotype networks with a very abundant and widespread central haplotype and a big number of singleton haplotypes, while their reconstructed demographic histories show a population expansion starting about 25-50 thousand years ago, a period marked by climate warming and increase in diatom abundance as inferred from bottom-lake sedimentary cores. CONCLUSIONS: In agreement with previous studies, we found that species reacted differently to the same environmental changes. Our results highlight the important role of dispersal ability and degree of ecological specialization in defining a species' response to environmental changes.