Population structure, adaptation and divergence of the meadow spittlebug, Philaenus spumarius (Hemiptera, Aphrophoridae), revealed by genomic and morphological data.

Eduardo Marabuto,Vinton Thompson,Paulo A.V. Borges,Ana Carina Neto,Chris D. Jiggins,Sofia G. Seabra,Maria Teresa Rebelo,Antti Halkka,Francisco Pina-Martins,Selçuk Yurtsever,Ana S.B. Rodrigues,Michael R. Wilson,Octávio S. Paulo,Sara E. Silva,José A. Quartau

doi:10.7717/peerj.11425

Abstract

Understanding patterns of population differentiation and gene flow in insect vectors of plant diseases is crucial for the implementation of management programs of disease. We investigated morphological and genome-wide variation across the distribution range of the spittlebug Philaenus spumarius (Linnaeus, 1758) (Hemiptera, Auchenorrhyncha, Aphrophoridae), presently the most important vector of the plant pathogenic bacterium Xylella fastidiosa Wells et al., 1987 in Europe. We found genome-wide divergence between P. spumarius and a very closely related species, P. tesselatus Melichar, 1899, at RAD sequencing markers. The two species may be identified by the morphology of male genitalia but are not differentiated at mitochondrial COI, making DNA barcoding with this gene ineffective. This highlights the importance of using integrative approaches in taxonomy. We detected admixture between P. tesselatus from Morocco and P. spumarius from the Iberian Peninsula, suggesting gene-flow between them. Within P. spumarius, we found a pattern of isolation-by-distance in European populations, likely acting alongside other factors restricting gene flow. Varying levels of co-occurrence of different lineages, showing heterogeneous levels of admixture, suggest other isolation mechanisms. The transatlantic populations of North America and Azores were genetically closer to the British population analyzed here, suggesting an origin from North-Western Europe, as already detected with mitochondrial DNA. Nevertheless, these may have been produced through different colonization events. We detected SNPs with signatures of positive selection associated with environmental variables, especially related to extremes and range variation in temperature and precipitation. The population genomics approach provided new insights into the patterns of divergence, gene flow and adaptation in these spittlebugs and led to several hypotheses that require further local investigation.

Highlights

Speciation involves the evolution of reproductive isolation and the buildup of genetic differentiation through selection and drift, but gene flow can counteract such divergence by homogenizing allelic variation and by allowing recombination to oppose or break associations between loci underlying isolating traits (Smadja & Butlin, 2011; Sousa & Hey, 2013)
Genome-wide analyses have allowed the detection of these ‘‘genomic islands’’ of differentiation in several systems (e.g., Malinsky et al, 2015; Vijay et al, 2016), other processes not related to speciation or reproductive isolation may be responsible for them, such as linked selection, variable recombination rates and/or density of targets of selection (Wolf & Ellegren, 2017)
The longer appendages in P. tesselatus are expected to be related to the longer body size in general in this species (Drosopoulos & Quartau, 2002) but, when controlling for the total length of the aedeagus, the relative size of the lower appendages remained larger in Moroccan samples (Fig. S2)

Summary

Introduction

Speciation involves the evolution of reproductive isolation and the buildup of genetic differentiation through selection and drift, but gene flow can counteract such divergence by homogenizing allelic variation and by allowing recombination to oppose or break associations between loci underlying isolating traits (Smadja & Butlin, 2011; Sousa & Hey, 2013). Several mechanisms may favour divergence in the face of gene flow, such as ecologically driven selection or sexual selection (Smadja & Butlin, 2011; Nosil, 2012). Genome-wide analyses have allowed the detection of these ‘‘genomic islands’’ of differentiation in several systems (e.g., Malinsky et al, 2015; Vijay et al, 2016), other processes not related to speciation or reproductive isolation may be responsible for them, such as linked selection, variable recombination rates and/or density of targets of selection (Wolf & Ellegren, 2017). Designated species may lie somewhere in this ‘‘speciation continuum’’, with different levels of divergence and gene flow (Hendry et al, 2009; Peccoud et al, 2009; Renaut et al, 2012; Riesch et al, 2017)

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Conclusion