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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.    Results  Populations showed marked genetic differentiation (average  F  ST  = 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 ( F  ST  = 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,    Conclusions  Populations 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.    Electronic supplementary material  The online version of this article (10.1186/s12862-018-1313-z) contains supplementary material, which is available to authorized users.

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