Abstract

Signatures of past changes in population size have been detected in genome-wide variation in many species. However, the causes of such demographic changes and the extent to which they are shared across co-distributed species remain poorly understood. During Pleistocene glacial maxima, many temperate European species were confined to southern refugia. While vicariance and range expansion processes associated with glacial cycles have been widely documented, it is unclear whether refugial populations of co-distributed species have experienced shared histories of population size change. We analyse whole-genome sequence data to reconstruct and compare demographic histories during the Quaternary for Iberian refuge populations in a single ecological guild (seven species of chalcid parasitoid wasps associated with oak cynipid galls). For four of these species, we find support for large changes in effective population size (Ne ) through the Pleistocene that coincide with major climate events. However, there is little evidence that the timing, direction and magnitude of demographic change are shared across species, suggesting that demographic histories in this guild are largely idiosyncratic, even at the scale of a single glacial refugium.

Highlights

  • Natural populations change in size and range in response to biotic and abiotic factors over both ecological and evolutionary timescales

  • We focus on the Iberian refugium, which for most species in the oak gall wasp parasitoid community—­including four out of the seven parasitoids studied here (Table 1)—r­epresents the end point of a longitudinal expansion history: Iberian populations have lower genetic diversity than more eastern refugia and show little evidence of population structure (Nicholls et al, 2010; Rokas et al, 2003; Stone et al, TA B L E 1 Maximum-­composite likelihood estimates (MCLE) of parameters under the single-­step-­change model for Iberian populations of seven species of chalcid parasitoid wasps under a model of a single-­step change

  • We address the following questions: (i) To what extent are the direction and timing of changes in Ne concordant across members of the oak gall parasitoid guild? Do species show evidence for simultaneous Ne change, suggesting concordant responses to a shared underlying driver, or are their demographic histories largely idiosyncratic as shown by Bunnefeld et al (2018) for the timing of divergence and admixture between refugia? (ii) Do sudden changes in population size coincide with specific glacial or interglacial periods in the Pleistocene? (iii) In species that have an Eastern origin, do the most drastic demographic changes occur after the colonization of Iberia, or are they shared with other refugial populations, suggesting that genetic diversity in Iberia largely reflects the size of the ancestral source populations?

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Summary

| INTRODUCTION

Natural populations change in size and range in response to biotic and abiotic factors over both ecological and evolutionary timescales. Bunnefeld et al (2018) used whole-­genome sequence data to compare the timing of divergence and admixture events between three southern refugial populations across 13 co-d­ istributed species in a tritrophic Western Palaearctic community comprising oak (Quercus) host plants, cynipid gall wasp herbivores and chalcid parasitoid natural enemies (Stone et al, 2002). The latter are obligate specialists of cynipid galls, allowing the guild of parasitoids to be considered in ecological isolation.

| MATERIALS AND METHODS
| RESULTS
| DISCUSSION
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