Gene flow in admixed populations and implications for the conservation of the Western honeybee, Apis mellifera

Abstract

Anthropogenic activity, especially modern apiculture, has considerable impact on the natural distribution of the Western honeybee, Apis mellifera, leading to the spread, replacement and fragmentation of many subspecies. This creates demand for the conservation of some subspecies, in particular, Apis mellifera mellifera, which once was widely distributed in Western Europe and nowadays is endangered through habitat loss and fragmentation. Moreover, A. m. mellifera may be further endangered by hybridisation in populations that now occur in artificial sympatry with other subspecies. Here, we quantify and compare individual hybridisation between sympatric and allopatric honeybee populations of A. m. mellifera and A. m. carnica using microsatellite markers and a Bayesian model-based approach. We had a special focus on pure breeding populations, which are a major tool in honeybee conservation. Our results demonstrate that subspecies are still highly differentiated, but gene flow is not prevented by the current management strategies, creating urgent demand for an improved conservation management of A. m. mellifera. However, the occurrence of a high number of pure individuals might suggest that some sort of hybrid barrier acts against the complete admixture of the two subspecies.

Developing reduced SNP assays from whole‐genome sequence data to estimate introgression in an organism with complex genetic patterns, the Iberian honeybee (Apis mellifera iberiensis)

“…Developing cost‐effective molecular tools for accurate estimation of introgression in A. mellifera is increasingly important as commercial strains (mostly of C‐lineage ancestry) are threatening native genetic diversity in many regions throughout Europe (Bertrand et al., 2015; De la Rúa et al., 2009; Jensen et al., 2005; Parejo et al., 2016; Pinto et al., 2014; Soland‐Reckeweg et al., 2009). In the postgenomics era, rapid innovations in high‐throughput sequencing technologies make it possible to construct extensive whole‐genome data sets, especially in model organisms with small genomes like the honeybee (Weinstock et al., 2006).…”

“…This human‐mediated gene flow has threatened A. m. mellifera, the other M‐lineage subspecies besides A. m. iberiensis in Europe. Indeed, the genetic integrity of A. m. mellifera has been compromised by introgressive hybridization and, in some areas, it has even been replaced by subspecies of C‐lineage ancestry (Jensen, Palmer, Boomsma, & Pedersen, 2005; Pinto et al., 2014; Soland‐Reckeweg, Heckel, Neumann, Fluri, & Excoffier, 2009). Yet, maintaining locally adapted subspecies is crucial for the long‐term sustainability of A. mellifera (De la Rúa et al., 2013; van Engelsdorp & Meixner, 2010).…”

“…A diverse array of molecular tools has been employed to monitor C‐lineage introgression including PCR‐RFLP of the intergenic tRNA leu ‐cox2 mtDNA region (Bertrand et al., 2015), microsatellites (Jensen et al., 2005; Soland‐Reckeweg et al., 2009) and, more recently, SNPs (Parejo et al., 2016; Pinto et al., 2014). Among these, SNPs are becoming the tool of choice for many applications because they are easily transferred between laboratories, have low genotyping error, provide high‐quality data, are suitable for automation in high‐throughput technologies (Vignal, Milan, SanCristobal, & Eggen, 2002), and are more powerful for estimating introgression in honeybees (Muñoz et al., 2017).…”

Using Whole-Genome Sequence Information to Foster Conservation Efforts for the European Dark Honey Bee, Apis mellifera mellifera

“…The large mating distances of drones and queens (Ruttner and Ruttner, 1972;Böttcher, 1975;Jensen et al, 2005b), as well as the highly polyandrous mating system (Woyke, 1964;Adams et al, 1977;Neumann et al, 1999b) impose practical difficulties to conserve honey bee subspecies or to maintain breeding lines (Neumann et al, 1999a). This is further confounded by the ease at which different subspecies hybridize with one another (Franck et al, 2000a;Soland-Reckeweg et al, 2009).…”

“…Islands or remote mountain valleys in particular offer excellent opportunities to limit the impact of non-native honey bees. Conservation measures usually include that introduced honey bees and hybrids are replaced by native bees after being identified by discrimination of wing morphology (Ruttner, 1988;Kauhausen-Keller and Keller, 1994) or genetic analyses using microsatellite markers (Neumann et al, 1999a;Scharpenberg et al, 2006;Soland-Reckeweg et al, 2009;Oleksa et al, 2011;Péntek-Zakar et al, 2015).…”