Autosomal and Mitochondrial Adaptation Following Admixture: A Case Study on the Honeybees of Reunion Island

Abstract

The honeybee population of the tropical Reunion Island is a genetic admixture of the Apis mellifera unicolor subspecies, originally described in Madagascar, and of European subspecies, mainly A. m. carnica and A. m. ligustica, regularly imported to the island since the late 19th century. We took advantage of this population to study genetic admixing of the tropical-adapted indigenous and temperate-adapted European genetic backgrounds. Whole genome sequencing of 30 workers and 6 males from Reunion, compared with samples from Europe, Madagascar, Mauritius, Rodrigues, and the Seychelles, revealed the Reunion honeybee population to be composed on an average of 53.2 ± 5.9% A. m. unicolor nuclear genomic background, the rest being mainly composed of A. m. carnica and to a lesser extent A. m. ligustica. In striking contrast to this, only 1 out of the 36 honeybees from Reunion had a mitochondrial genome of European origin, suggesting selection has favored the A. m. unicolor mitotype, which is possibly better adapted to the island’s bioclimate. Local ancestry was determined along the chromosomes for all Reunion samples, and a test for preferential selection for the A. m. unicolor or European background revealed 15 regions significantly associated with the A. m. unicolor lineage and 9 regions with the European lineage. Our results provide insights into the long-term consequences of introducing exotic specimen on the nuclear and mitochondrial genomes of locally adapted populations.

Genetic past, present, and future of the honey bee (Apis mellifera) in the United States of America

“…Second, honey bees in their introduced range in the USA and their native range have experienced declines in genetic diversity due to Varroa mites (Bozek et al 2018;Espregueira Themudo et al 2020). Finally, only 13 honey bee subspecies have been sequenced to date (Chen et al 2016;Haddad et al 2018;Harpur et al 2014;Wallberg et al 2014Wallberg et al , 2017Wragg et al 2018;Yunusbaev et al 2019) and the sequencing has been performed using different sequencing technologies, complicating the direct comparison of data sets (Cridland et al 2017). This has limited not only our ability to cleanly compare levels of genetic diversity but also our ability to estimate relatedness of samples in the USA to samples within the honey bee's native range.…”

“…3; Table S3). This is also true of honey bees in their native ranges: only 13 of 29 subspecies have been sequenced (Chen et al 2016;Haddad et al 2018;Wallberg et al 2014Wallberg et al , 2017Wragg et al 2018). This incomplete record-in both areas-prevents us from fully identifying the origins of haplotypes present within US populations.…”

Whole-Genome Sequence Analysis of Italian Honeybees (Apis mellifera)

“…Some are based on the use of morphometric analyses on the wing venation [ 11 ]. Concerning DNA analysis, studies have been conducted with microsatellites [ 6 , 13 , 14 ], and mitochondrial DNA [ 7 , 10 , 15 , 16 , 17 ]. Early studies conducted on the Italian populations found hybridization events between the A.m. ligustica and A.m. mellifera subspecies on the Ligurian coast and along the western Alpine arch [ 18 ] by analyzing allozymes at the Mdh-1 locus.…”

“…Thanks to its favorable characteristics, this subspecies has spread since 1800 in many other regions of the world by human mediated action. Today, specimens of A.m. ligustica can be found in North America, in northern and central Europe [5,6], in Reunion island [7], in Kangaroo Island in southern Australia [8], in China [9], in Mauritius island [10] and in Brazil [11].…”

Complex population structure and haplotype patterns in Western Europe honey bee from sequencing a large panel of haploid drones

“…As no high-density SNP chip was available for honey bee at the onset of the project, and as the honey bee genome is very small compared to most animal genomes, being only 226.5 Mb long [33], we employed a whole-genome sequencing approach [28,34]. Although the sequencing of honey bee workers has proved successful for detecting selection signatures or admixture events [28,[34][35][36], analysing haploid drones allows to sequence at a lower depth and with greater accuracy in variant detection [20,29,31]. An additional advantage of sequencing haploids is that the alleles are phased, which is invaluable for studies investigating genome dynamics such as recombination hotspots and haplotype structure.…”