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Revisiting the Iberian honey bee (Apis mellifera iberiensis) contact zone: maternal and genome-wide nuclear variations provide support for secondary contact from historical refugia

Publication . Chávez-Galarza, Julio; Henriques, Dora; Johnston, J. Spencer; Carneiro, Miguel; Rufino, José; Patton, John C.; Pinto, M. Alice

Dissecting diversity patterns of organisms endemic to Iberia has been truly challenging for a variety of taxa, and the Iberian honey bee is no exception. Surveys of genetic variation in the Iberian honey bee are among the most extensive for any honey bee subspecies. From these, differential and complex patterns of diversity have emerged, which have yet to be fully resolved. Here, we used a genome-wide data set of 309 neutrally tested single nucleotide polymorphisms (SNPs), scattered across the 16 honey bee chromosomes, which were genotyped in 711 haploid males. These SNPs were analysed along with an intergenic locus of the mtDNA, to reveal historical patterns of population structure across the entire range of the Iberian honey bee. Overall, patterns of population structure inferred from nuclear loci by multiple clustering approaches and geographic cline analysis were consistent with two major clusters forming a well-defined cline that bisects Iberia along a northeastern-southwestern axis, a pattern that remarkably parallels that of the mtDNA. While a mechanism of primary intergradation or isolation by distance could explain the observed clinal variation, our results are more consistent with an alternative model of secondary contact between divergent populations previously isolated in glacial refugia, as proposed for a growing list of other Iberian taxa. Despite current intense honey bee management, human-mediated processes have seemingly played a minor role in shaping Iberian honey bee genetic structure. This study highlights the complexity of the Iberian honey bee patterns and reinforces the importance of Iberia as a reservoir of Apis mellifera diversity.

2015Journal article

Open access

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)

Publication . Henriques, Dora; Parejo, Melanie; Vignal, Alain; Wragg, David; Wallberg, Andreas; Webster, Matthew T.; Pinto, M. Alice

The most important managed pollinator, the honeybee (Apis mellifera L.), has been subject to a growing number of threats. In western Europe, one such threat is large- scale introductions of commercial strains (C- lineage ancestry), which is leading to introgressive hybridization and even the local extinction of native honeybee populations (M- lineage ancestry). Here, we developed reduced assays of highly informative SNPs from 176 whole genomes to estimate C- lineage introgression in the most diverse and evolutionarily complex subspecies in Europe, the Iberian honeybee (Apis mellifera iberiensis). We started by evaluating the effects of sample size and sampling a geographically restricted area on the number of highly informative SNPs. We demonstrated that a bias in the number of fixed SNPs (FST = 1) is introduced when the sample size is small (N ≤ 10) and when sampling only captures a small fraction of a population’s genetic diversity. These results underscore the importance of having a representative sample when developing reliable reduced SNP assays for organisms with complex genetic patterns. We used a training data set to design four independent SNP assays selected from pairwise FST between the Iberian and C- lineage honeybees. The designed assays, which were validated in holdout and simulated hybrid data sets, proved to be highly accurate and can be readily used for monitoring populations not only in the native range of A. m. iberiensis in Iberia but also in the introduced range in the Balearic islands, Macaronesia and South America, in a time- and cost- effective manner. While our approach used the Iberian honeybee as model system, it has a high value in a wide range of scenarios for the monitoring and conservation of potentially hybridized domestic and wildlife populations.

2018Journal article

Open access

Adaptação local na abelha ibérica

Publication . Henriques, Dora; Wallberg, Andreas; Chávez-Galarza, Julio; Neves, Cátia J.; Costa, Filipe Oliveira; Webster, Matthew T.; Pinto, M. Alice

Perceber a base genética do processo de adaptação permite uma previsão de como os organismos poderão responder a mudanças ambientais. A sequenciação de genomas a baixo custo, juntamente com os avanços das ferramentas estatísticas e computacionais possibilitam a compreensão da base genética da adaptação. O objectivo deste trabalho é o estudo da adaptação local da abelha ibérica, tendo como base algoritmos que permitem a incorporação de dados genéticos e ambientais. A Península Ibérica constituiu um local de interesse para este tipo de estudos por ser constituída por uma diversidade climática como Mediterrânico e Atlântico. Foram sequenciados 86 genomas de indivíduos distribuídos em 3 transectos (Atlântico, Central e Mediterrâneo) de forma a representar a diversidade climática existente na Península Ibérica. Em cada ponto de amostragem os dados de latitude e longitude foram recolhidos e variáveis ambientais foram retiradas das bases de dados WorldClim e Climatic Research Unit. Os métodos LFMM e Samβada, que integram informação genética e ambiental foram utilizados para procurar sinais de selecção. A vantagem destes métodos é que se pode perceber quais as variáveis ambientais que exercem uma pressão selectiva e que genes estão associados a cada variável. No total foram identificados 1289449 SNPs, dos quais 2193 mostraram estar significativamente associados com variáveis ambientais. Estes estão localizados em 826 genes. No conjunto das variáveis ambientais utilizadas, a longitude, latitude e precipitação apresentaram um maior num de SNPs associados. Foram encontrados genes com diversas funções, por exemplo quatro genes parecem relacionados com o desenvolvimento do sistema imunitário e este encontram associados à longitude, para a latitude proteínas de ligação parecem ser predominantes, já na precipitação aparecem genes relacionados com a morfogénese, actividade transportadora transmembranar e actividade olfactória. Este estudo representa primeira tentativa de compreender a base genética da adaptação local a partir de genomas completos.

2016Conference object

Open access

Reduced SNP panels for genetic identification and introgression analysis in the dark honey bee (Apis mellifera mellifera)

Publication . Muñoz, Irene; Henriques, Dora; Johnston, J. Spencer; Chávez-Galarza, Julio; Kryger, Per; Pinto, M. Alice

Beekeeping activities, especially queen trading, have shaped the distribution of honey bee (Apis mellifera) subspecies in Europe, and have resulted in extensive introductions of two eastern European C-lineage subspecies (A. m. ligustica and A. m. carnica) into the native range of the M-lineage A. m. mellifera subspecies in Western Europe. As a consequence, replacement and gene flow between native and commercial populations have occurred at varying levels across western European populations. Genetic identification and introgression analysis using molecular markers is an important tool for management and conservation of honey bee subspecies. Previous studies have monitored introgression by using microsatellite, PCR-RFLP markers and most recently, high density assays using single nucleotide polymorphism (SNP) markers. While the latter are almost prohibitively expensive, the information gained to date can be exploited to create a reduced panel containing the most ancestry-informative markers (AIMs) for those purposes with very little loss of information. The objective of this study was to design reduced panels of AIMs to verify the origin of A. m. mellifera individuals and to provide accurate estimates of the level of C-lineage introgression into their genome. The discriminant power of the SNPs using a variety of metrics and approaches including the Weir & Cockerham's FST, an FST-based outlier test, Delta, informativeness (In), and PCA was evaluated. This study shows that reduced AIMs panels assign individuals to the correct origin and calculates the admixture level with a high degree of accuracy. These panels provide an essential tool in Europe for genetic stock identification and estimation of admixture levels which can assist management strategies and monitor honey bee conservation programs.

2015Journal article

Open access

Maternal structure of Iberian honey bees inferred from whole mitochondrial genomes

Publication . Henriques, Dora; Chávez-Galarza, Julio; Patton, John C.; Rufino, José; Pinto, M. Alice

The maternally inherited mitochondrial DNA has been the marker of choice for assessing Iberian honey bee variation, particularly the intergenic tRNA leu -cox2 region. The data generated by massive sampling of this region confirmed early findings of coexistence of African (A) and western European (M) lineages, forming a southwestern–northeastern cline, and revealed unparalleled levels of haplotype diversity and complexity. Accordingly, it has been suggested that Iberia served as a glacial refuge, and as a place of secondary contact between European and African lineages. While we have learned a great deal with this region, due to its high levels of variation and repetitive structure, there are evolutionary questions that an only be properly addressed using other mitochondrial regions. In this study, we used NGS technology to sequence the mitogenomes of 92 individuals and analyzed the data using two phylogenetic methods.

2014Conference object

Open access