Abstract

Many animal species experiencing spatial or interannual fluctuations of their environment are capable of prolonged diapause, a kind of dormancy that extends over more than one year. Such a prolonged diapause is commonly perceived as a temporal demographic refuge in stochastic environments, but empirical evidence is still lacking of its consequences on temporal population genetic structures. In this long-term study, we investigated how a particular pattern of prolonged diapause may influence the temporal population genetics of the invasive seed-specialized wasp Megastigmus schimitscheki (Hymenoptera: Torymidae) in southeastern France. We characterized the diapause strategy of M. schimitscheki using records of emergence from diapause in 97 larval cohorts, and we conducted a temporal population genetic study on a natural invasive wasp population sampled during ten consecutive years (1999–2008) using polymorphic microsatellite markers. We found that M. schimitscheki can undergo a prolonged diapause of up to five years and displays two main adult emergence peaks after two and four years of diapause. Such a bimodal and atypical pattern did not disrupt temporal gene flow between cohorts produced in even and in odd years during the period of the study. Unexpectedly, we found that this wasp population consisted of two distinct genetic sub-populations that strongly diverged in their diapause strategies, with very few admixed individuals. One of the sub-populations displayed both short and prolonged diapause (2 and 4 years respectively) in equal proportions, whereas the other sub-population displayed mainly short diapause. This study provided empirical evidence that prolonged diapause phenotypes can substantially contribute to reproduction and impact temporal genetic structures. Prolonged diapause is likely to act as both demographic and genetic refuges for insect populations living in fluctuating environments.

Highlights

  • In species living in seasonal and stochastic environments, life cycle traits are strongly selected to respond to the spatial and temporal heterogeneity of abiotic and/or biotic environmental factors [1], [2]

  • Pattern of Diapause in M. schimitscheki Emergences of M. schimitscheki spread over a maximum of five years in each cohort, i.e., adult emergences from cohorts produced at a year n (1999–2007) could be recorded at n+2 (2001–2009), n+3 (2002–2010), n+4 (2003–2011) and n+5 (2004–2012), indicating that a fraction of each cohort could have a diapause prolonged by 1, 2 or 3 years (Figure 2)

  • To assess whether the bimodal pattern of diapause was specific to M. schimitscheki or a common feature in wasp species exploiting true cedars, propensity to prolonged diapause was estimated in the closely related species M. pinsapinis, which lives in sympatry with M. schimitscheki in southeastern France and exploits the same ecological niche

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Summary

Introduction

In species living in seasonal and stochastic environments, life cycle traits are strongly selected to respond to the spatial and temporal heterogeneity of abiotic and/or biotic environmental factors [1], [2]. A kind of dormancy shown to play a key role in the evolution of life histories of animal species, has been described as an integrated response to predictable environmental fluctuations, allowing survival during portions of the year that are inappropriate for growth and reproduction [1], [3], [4]. When conditions are less predictable and species experience severe spatial or interannual fluctuations of their environment diapause may extend over more than one year [5,6,7]. Such a prolonged diapause is viewed as a temporal dispersal strategy [6], [8]. In most cases environmental conditions are less predictable and emergences of a cohort are spread over several years, with a higher proportion of individuals emerging after the minimum diapause duration (obligatory diapause) and decreasing proportions of individuals emerging over the following years [2], [6], [14]

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