Low Spontaneous Mutation Rate and Pleistocene Radiation of Pea Aphids

Abstract

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.

The first steps toward a global pandemic: Reconstructing the demographic history of parasite host switches in its native range

“…By promoting genomic heterogeneity and introducing beneficial mutations (Tomasini and Peischl 2020), gene flow can ameliorate lost diversity due to selection or inbreeding (Lenormand 2002; Whiteley et al 2015), both of which would impact host-switched Varroa populations. Alternatively, de novo mutation rates could contribute to population genetic variation, but our direct estimation of mutation rate did not show exceptionally high mutation rates (< 8 × 10 -10 per bp per generation), compared to other arthropods (H. Liu et al 2017; Fazalova and Nevado 2020). Consequently, immigration may be the primary means of introducing new alleles into populations on the novel host during early stages of the host switch.…”

“…Given that we were only able to estimate the upper limit of de novo mutation rate, we explored whether lower mutation rate improve the observed maximum likelihood distribution of 100 replicates (Figure S1). We examined rates as low as 1.0 × 10 -11 , at the lower limit of rates in arthropods (Fazalova and Nevado 2020). We also tested whether including an inbreeding coefficient would help improving the model likelihood by implement 70% of inbreeding (minimum detected in both species).…”

The first steps toward a global pandemic: Reconstructing the demographic history of parasite host switches in its native range

“…By promoting genomic heterogeneity and introducing bene cial mutations (Tomasini and Peischl 2020), gene ow can ameliorate lost diversity due to selection or inbreeding (Lenormand 2002;Whiteley et al 2015), both of which would impact host-switched Varroa populations. Alternatively, de novo mutation rates could contribute to population genetic variation, but our direct estimation of mutation rate did not show exceptionally high mutation rates (< 8 × 10 -10 per bp per generation), compared to other arthropods (H. Liu et al 2017;Fazalova and Nevado 2020). Consequently, immigration may be the primary means of introducing new alleles into populations on the novel host during early stages of the host switch.…”

Wing plasticity and associated gene expression varies across the pea aphid biotype complex

“…The pea aphid species complex comprises multiple populations, termed ‘biotypes,’ that began diverging approximately 500,000 years ago (Fazalova and Nevado 2020; but see Peccoud et al. 2009b) and are to different degrees adapted to host plants within the family Fabaceae (Ferrari et al.…”