Small and genetically highly structured populations in a long-legged bee, Rediviva longimanus, as inferred by pooled RAD-seq

Belinda Kahnt,Panagiotis Theodorou,Robert J Paxton,Michael Kuhlmann,Hilke Hollens-Kuhr,Anton Pauw,Antonella Soro

doi:10.1186/s12862-018-1313-z

Abstract

Adaptation to local host plants may impact a pollinator’s population genetic structure by reducing gene flow and driving population genetic differentiation, representing an early stage of ecological speciation. South African Rediviva longimanus bees exhibit elongated forelegs, a bizarre adaptation for collecting oil from floral spurs of their Diascia hosts. Furthermore, R. longimanus foreleg length (FLL) differs significantly among populations, which has been hypothesised to result from selection imposed by inter-population variation in Diascia floral spur length. Here, we used a pooled restriction site-associated DNA sequencing (pooled RAD-seq) approach to investigate the population genetic structure of R. longimanus and to test if phenotypic differences in FLL translate into increased genetic differentiation (i) between R. longimanus populations and (ii) between phenotypes across populations. We also inferred the effects of demographic processes on population genetic structure and tested for genetic markers underpinning local adaptation.ResultsPopulations showed marked genetic differentiation (average FST = 0.165), though differentiation was not statistically associated with differences between populations in FLL. All populations exhibited very low genetic diversity and were inferred to have gone through recent bottleneck events, suggesting extremely low effective population sizes. Genetic differentiation between samples pooled by leg length (short versus long) rather than by population of origin was even higher (FST = 0.260) than between populations, suggesting reduced interbreeding between long and short-legged individuals. Signatures of selection were detected in 1119 (3.8%) of a total of 29,721 SNP markers,ConclusionsPopulations of R. longimanus appear to be small, bottlenecked and isolated. Though we could not detect the effect of local adaptation (FLL in response to floral spurs of host plants) on population genetic differentiation, short and long legged bees appeared to be partially differentiated, suggesting incipient ecological speciation. To test this hypothesis, greater resolution through the use of individual-based whole-genome analyses is now needed to quantify the degree of reproductive isolation between long and short legged bees between and even within populations.

Highlights

Mating usually takes place among a subset of individuals of a species, typically within a portion of its distributional range, and, assuming limited dispersal, populations of that species inevitably become genetically structured [1]
We used a pooled restriction site-associated DNA sequencing approach to investigate the population genetic structure of R. longimanus and to test if phenotypic differences in foreleg length (FLL) translate into increased genetic differentiation (i) between R. longimanus populations and (ii) between phenotypes across populations
Though we could not detect the effect of local adaptation (FLL in response to floral spurs of host plants) on population genetic differentiation, short and long legged bees appeared to be partially differentiated, suggesting incipient ecological speciation

Summary

Introduction

Mating usually takes place among a subset of individuals of a species, typically within a portion of its distributional range, and, assuming limited dispersal, populations of that species inevitably become genetically structured [1]. Adaptation to different host plant morphologies might hinder genetic exchange between insect populations and generate strong barriers to gene flow [14]. Such populations may accumulate allele frequency differences, i.e. become genetically differentiated, often assessed via FST, which relates the amount of genetic variation among populations to the total genetic variation over all populations [15]. Increased genetic differentiation is expected at loci underlying local adaptation whereas ecologically neutral loci are not subject to divergent selection and should show less differentiation This generates a heterogeneous pattern of genomic divergence characterised by ‘islands of genomic divergence’ containing FST outlier loci [16, 17]. Host plant mediated genetic differentiation and incipient ecological speciation have been suggested for several insects [4, 5, 9, 19, 20]

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