Varying degrees of Apis mellifera ligustica introgression in protected populations of the black honeybee, Apis mellifera mellifera, in northwest Europe

Abstract

The natural distribution of honeybee subspecies in Europe has been significantly affected by human activities during the last century. Non-native subspecies of honeybees have been introduced and propagated, so that native black honeybee (Apis mellifera mellifera) populations lost their identity by gene-flow or went extinct. After previous studies investigated the remaining gene-pools of native honeybees in France and Spain, we here assess the genetic composition of eight northwest European populations of the black honeybee, using both mitochondrial (restriction fragment length polymorphisms of the intergenic transfer RNAleu-COII region) and nuclear (11 microsatellite loci) markers. Both data sets show that A. m. mellifera populations still exist in Norway, Sweden, Denmark, England, Scotland and Ireland, but that they are threatened by gene flow from commercial honeybees. Both Bayesian admixture analysis of the microsatellite data and DraI-RFLP (restriction fragment length polymorphism) analysis of the intergenic region indicated that gene-flow had hardly occurred in some populations, whereas almost 10% introgression was observed in other populations. The most introgressed population was found on the Danish Island of Laeso, which is the last remaining native Danish population of A. m. mellifera and the only one of the eight investigated populations that is protected by law. We discuss how individual admixture analysis can be used to monitor the restoration of honeybee populations that suffer from unwanted hybridization with non-native 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).…”

“…Unlike many populations of A. m. mellifera from western Europe and A. m. iberiensis from the archipelagos of Baleares and Macaronesia , which are threatened by human‐mediated gene flow (De la Rúa et al., 2001, 2003; Jensen et al., 2005; Miguel et al., 2015; Muñoz et al., 2014; Pinto et al., 2014), there is very limited introgression in A. m. iberiensis populations of Iberia (Chávez‐Galarza et al., 2015). Therefore, it is crucial to monitor Iberian populations, before gene complexes shaped by natural selection over evolutionary time are irretrievably lost.…”

“…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).…”

Asymmetric hybridization of Primula secundiflora and P. poissonii in three sympatric populations

“…自然杂交是指两个遗传上不同的居群之间的 交配繁殖 (Barton & Hewitt, 1985), 是动植物中一种 常见的现象(Arnold, 1997)。由于揭示自然杂交事件 有利于深入理解生殖隔离的机制和进化 (Zhou et al, 2008), 近几十年来它吸引了众多学者的目光 (Anderson, 1948;Mallet, 2005;van Droogenbroeck et al, 2006;Arnold et al, 2012;Abbott et al, 2013)。自然杂 交可能会引起诸多遗传后果, 比如渐渗杂交可能会 促进种间基因流并产生新的基因型组合, 从而增加 物种的分化和生态适应性 (Ellstrand et al, 1999;Jensen et al, 2005;Abbott et al, 2013); 过度的种间杂 交则可能导致遗传融合, 降低物种多样性 (Levin et al, 1996;Runyeon-Lager & Prentice, 2000)。 杂交的 方向是杂交中一个非常重要的方面 (Zhou et al, 2008), 在杂交过程中, 杂交方向可能是不对称的双 向杂交或单向杂交。这种现象在植物中相对比较常 见 (Zha et al, 2010;Field et al, 2011;Muranishi et al, 2013;Zhang et al, 2016)。而造成这种现象的原因有 很多, 比如单向不亲和(unilateral incompatibility)、 开花物候、传粉昆虫的选择偏好以及亲本在同域居 群中的分布数量 (Carney et al, 2000;Zhou et al, 2008;Zha et al, 2010;Muranishi et al, 2013; (Du et al, 2012;Yu et al, 2014;Liao et al, 2015), 甚至可通过自然杂交形成新的物种 (Arnold & Richards, 1998;Richards, 2003;Wu & Zhang, 2010)。 自然杂交事件在报春花属的很多分 布范围内被广泛记载 (Stace, 1975;Richards, 2003;Zhu et al, 2009;Terzioglu et al, 2012;Ma et al, 2014)。 但目前在我国西南地区仅报道两例报春花属 植物的自然杂交事件 (Zhu et al, 2009;Ma et al, 2014) 图3 基于Bayes法构建的核转录间隔区ITS和叶绿体基因trnH-psbA系统树。GZ、PTS和SABG分别代表格咱乡、普达措国 家公园和香格里拉高山植物园居群。 Fig. 3 The nuclear ITS and chloroplast trnH-psbA phylogeny tree based on Bayes method.…”