POPULATION GENOMICS AND LANDSCAPE GENETICS OF THE IBERIAN HONEY BEE APIS MELLIFERA IBERIENSIS

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Publications

Signatures of selection in the Iberian honey bee (Apis mellifera iberiensis) revealed by a genome scan analysis of single nucleotide polymorphisms (SNPs)

Publication . Chávez-Galarza, Julio; Henriques, Dora; Johnston, J. Spencer; Azevedo, João; Patton, John C.; Muñoz, Irene; De la Rúa, Pilar; Pinto, M. Alice

Understanding the genetic mechanisms of adaptive population divergence is one of the most fundamental endeavours in evolutionary biology and is becoming increasingly important as it will allow predictions about how organisms will respond to global environmental crisis. This is particularly important for the honey bee, a species of unquestionable ecological and economical importance that has been exposed to increasing human-mediated selection pressures. Here, we conducted a single nucleotide polymorphism (SNP)-based genome scan in honey bees collected across an environmental gradient in Iberia and used four FST-based outlier tests to identify genomic regions exhibiting signatures of selection. Additionally, we analysed associations between genetic and environmental data for the identification of factors that might be correlated or act as selective pressures. With these approaches, 4.4% (17 of 383) of outlier loci were cross-validated by four FST-based methods, and 8.9% (34 of 383) were cross-validated by at least three methods. Of the 34 outliers, 15 were found to be strongly associated with one or more environmental variables. Further support for selection, provided by functional genomic information, was particularly compelling for SNP outliers mapped to different genes putatively involved in the same function such as vision, xenobiotic detoxification and innate immune response. This study enabled a more rigorous consideration of selection as the underlying cause of diversity patterns in Iberian honey bees, representing an important first step towards the identification of polymorphisms implicated in local adaptation and possibly in response to recent human-mediated environmental changes.

2013Journal article

Open access

Unraveling the local adaptation and population structure of Iberian honey bee

Publication . Chávez-Galarza, Julio; Costa, Filipe Oliveira; Pinto, M. Alice

Unraveling the complex evolutionary history of Apis mellifera iberiensis is a challenging task. Several studies have been carried out in the Iberian honey bee to explain its origin, suggesting two possible hypotheses: a primary intergradation process (morphology and allozymes), or a secondary contact process (mtDNA) supported by an abrupt southwestern-northeastern cline formed by two divergent lineages. Surveys with microsatellites support neither hypothesis. The goal of this work is to unravel the evolutionary history of the Iberian honey bee using SNPs. To that end, 711 individuals of A. m. iberiensis were collected in 23 sites across three north-south transepts in the Iberian Peninsula. This collection was genotyped for 1536 SNPs using the GoldenGate assay of Illumina. The SNP dataset was examined in search for signatures of selection by coalescence, Bayesian and spatial analysis. Then, the population structure was inferred by using Bayesian methods and multivariate and spatial analysis. Analysis of selection detected 10 loci exhibiting strong selection signal. Their putative functions were determined using the honey bee genomic resources and mapped to putative genes with diverse biological functions, which included vision, detoxification metabolism, and immunity. On the other hand, the population structure recovers the cline southwestern-northeastern found using mtDNA markers.

2013Conference object

Open access

Análisis de introgresión en Apis mellifera iberiensis y Apis mellifera mellifera usando polimorfismos de nucleótidos simples (SNPs)

Publication . Chávez-Galarza, Julio; Henriques, Dora; Johnston, J. Spencer; Rufino, José; Pinto, M. Alice

Diferentes estudios han agrupado las subespecies de A. mellifera en cuatro linajes evolutivos basados sobre marcadores morfométricos, ecológicos, microsatélites y mtDNA: Africano (A), Medio Oriente (O), Este y Centro de Europa (C), Norte y Oeste de Europa (M). El linaje M está representado por las subespecies A. m. iberiensis y A. m. mellifera, cuya distribución es la Península Ibérica para la primera y desde los Pirineos hacia el Norte de Europa para la segunda. Durante las últimas décadas, la introducción masiva de subespecies del linaje C por apicultores ha ocasionado un fuerte flujo génico y más aún al casi completo remplazamiento de A. m. mellifera, como ha sido reportado para Alemania. Por tanto, el análisis de niveles de introgresión en programas de crianza y conservación es de vital importancia para evitar la perdida de diversidad genética y sustitución de especies nativas. Este estudio busca identificar los niveles de introgresión de subespecies del linaje C en las subespecies pertenecientes al linaje M a través de un análisis amplio del genoma usando SNPs. Para 711 individuos correspondiente a A. m. iberiensis y 88 individuos A. m. mellifera fueron genotipados 1536 SNPs. Las subespecies de linaje C A. m. ligustica y A. m. carnica fueron usados como poblaciones de referencia. Los niveles de introgresión fueron evaluados usando un método de agrupamiento Bayesiano implementado en el software STRUCTURE. Nuestros resultados indicaron que la introgresión en A. m .iberiensis no es significante, a diferencia en A. m. mellifera que presentó de 8% a 30% de introgresión. Considerando que muchas de las muestras de A. m. mellifera son provenientes de poblaciones integradas en programas de conservación en el Norte de Europa, este resultado evidencia el profundo contraste entre las dos subespecies del linaje M con respecto a su estado de conservación.

2014Conference object

Open access

SNPs selected by information content outperform randomly selected microsatellite loci for delineating genetic identification and introgression in the endangered dark European honeybee (Apis mellifera mellifera)

Publication . Muñoz, Irene; Henriques, Dora; Jara, Laura; Johnston, J. Spencer; Chávez-Galarza, Julio; De la Rúa, Pilar; Pinto, M. Alice

The honeybee (Apis mellifera) has been threatened by multiple factors including pests and pathogens, pesticidesand loss of locally adapted gene complexes due to replacement and introgression. In western Europe, the geneticintegrity of the native A. m. mellifera (M-lineage) is endangered due to trading and intensive queen breeding withcommercial subspecies of eastern European ancestry (C-lineage). Effective conservation actions require reliablemolecular tools to identify pure-bred A. m. mellifera colonies. Microsatellites have been preferred for identiﬁcationof A. m. mellifera stocks across conservation centres. However, owing to high throughput, easy transferabilitybetween laboratories and low genotyping error, SNPs promise to become popular. Here, we compared the resolvingpower of a widely utilized microsatellite set to detect structure and introgression with that of different sets that com-bine a variable number of SNPs selected for their information content and genomic proximity to the microsatelliteloci. Contrary to every SNP data set, microsatellites did not discriminate between the two lineages in the PCA space.Mean introgression proportions were identical across the two marker types, although at the individual level,microsatellites’ performance was relatively poor at the upper range of Q-values, a result reﬂected by their lower pre-cision. Our results suggest that SNPs are more accurate and powerful than microsatellites for identiﬁcation of A. m.mellifera colonies, especially when they are selected by information content.

2017Journal article

Open access

Effect of linkage disequilibrium on inferences of population structure and introgression of iberian and black honey bees

Publication . Chávez-Galarza, Julio; Henriques, Dora; Kryger, Per; De la Rúa, Pilar; Johnston, J. Spencer; Rufino, José; Pinto, M. Alice

Identification of population structure, a primary goal in population genetics, is easily performed because there is a number of methods available, implemented by user-friendly software packages. However, the user must be cautious when inferring population structure because spurious results may be obtained when there is strong linkage disequilibrium. With recent development of high-density SNPs we have now more power to interrogate the honey bee genome. However, the greater the number of loci genotyped the greater the chance of scoring loci that are linked. In addition, events such as population bottleneck, small effective population size, genetic drift, and admixture may also generate strong linkage disequilibrium. According to Kaeuffer et al. (2007), correlation rLD is the best way to deal with linkage disequilibrium. These authors recommend removing loci with rLD higher than 0.5 when inferring structure. In this study we used the GoldenGate Assay of Illumina to genotype over 1221 loci in individuals sampled from populations of A.m. iberiensis and A.m. mellifera. In this dataset we used the genetic distance between SNPs and rLD to test the effect of linkage in the number of clusters and the introgression level inferred by the clustering method implemented in the software STRUCTURE.

2012Conference object

Open access