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Every year more than 1 million commercial bumblebee colonies are deployed in greenhouses worldwide for their pollination services. While commercial pollinators have been an enormous benefit for crop production, their use is emerging as an important threat. Commercial pollinators have been linked to pathogen spillover, and their introduction outside their native area has had devastating effects on native pollinators. A more pervasive but underappreciated threat is their potential impact on the genetic integrity of native pollinators. We set up a sampling and genotyping‐plus‐phenotyping protocol to evaluate the presence and extent of hybridization between commercial and native individuals of Bombus terrestris in south‐western Spain, a region experiencing a huge propagule pressure of non‐native genotypes due to the massive use of commercial colonies for crop pollination. Our genomic data show clear evidence of generalized hybridization between native and introduced commercial bumblebee lineages in southern Spain. Only 19% of analysed individuals were assigned with high confidence to the pure native genetic cluster and >45% of sampled specimens were first‐generation hybrids or backcrosses between native and commercial genotypes, indicating that genetic introgression is pervasive in southern Spain. Although the frequency of commercial genotypes sharply declined with the distance to greenhouses, non‐native alleles have introgressed into native populations inhabiting protected natural parks >60 km away from commercial bumblebee release areas. As pollination services demand will increase in the coming years, only a more restrictive regulation of commercial lines could mitigate their negative impacts on the genetic integrity of native pollinators, avoid processes of genetic homogenization, and prevent the potential disruption of local adaptations. (Spanish) Cada año, más de un millón de colonias comerciales de abejorros se colocan en invernaderos de todo el mundo para aprovechar sus servicios como polinizadores. Si bien los polinizadores comerciales han sido un enorme beneficio para la producción de cultivos, su uso se está convirtiendo en una amenaza importante. Los polinizadores comerciales se han relacionado con la propagación de patógenos y su introducción fuera de su área nativa ha tenido efectos devastadores en los polinizadores nativos. Una amenaza más generalizada pero poco apreciada es su impacto potencial en la integridad genética de los polinizadores nativos. Establecimos un protocolo de muestreo y genotipado más fenotipado para evaluar la presencia y el alcance de la hibridación entre individuos comerciales y nativos de Bombus terrestris en el suroeste de España, una región que experimenta una enorme presión de propágulos de genotipos no nativos debido al uso masivo de colonias comerciales para la polinización de cultivos. Nuestros datos genómicos muestran evidencia clara de hibridación generalizada entre linajes de abejorros comerciales nativos e introducidos en el sur de España. Solo el 19% de los individuos analizados fueron asignados con una alta confianza al grupo genético nativo puro y > 45% de los especímenes muestreados eran híbridos o retrocruces de primera generación entre genotipos nativos y comerciales, lo que indica que la introgresión genética es generalizada en el sur de España. Aunque la frecuencia de los genotipos comerciales disminuyó drásticamente con la distancia a los invernaderos, los alelos no nativos se han intrigado en las poblaciones nativas que habitan en parques naturales protegidos > 60 km de distancia de las áreas comerciales donde se liberan de abejorros. Como la demanda de servicios de polinización aumentará en los próximos años, solo una regulación más restrictiva de las líneas comerciales podría mitigar sus impactos negativos sobre la integridad genética de los polinizadores nativos, evitar procesos de homogeneización genética y prevenir la perdida potencial de las adaptaciones locales. Wild and commercial bumblebees from different subspecies are hybridizing. This genetic introgression is widespread and threatens local adaptations. Stronger regulations are needed to safeguard pollinators' genetic diversity.

Background Species thermal requirements are one of the principal determinants of their ecology and biogeography, although our understanding of the interplay between these factors is limited by the paucity of integrative empirical studies. Here we use empirically collected thermal tolerance data in combination with molecular phylogenetics/phylogeography and ecological niche modelling to study the evolution of a clade of three western Mediterranean diving beetles, the Agabus brunneus complex. Results The preferred mitochondrial DNA topology recovered A. ramblae (North Africa, east Iberia and Balearic islands) as paraphyletic, with A. brunneus (widespread in the southwestern Mediterranean) and A. rufulus (Corsica and Sardinia) nested within it, with an estimated origin between 0.60-0.25 Ma. All three species were, however, recovered as monophyletic using nuclear DNA markers. A Bayesian skyline plot suggested demographic expansion in the clade at the onset of the last glacial cycle. The species thermal tolerances differ significantly, with A. brunneus able to tolerate lower temperatures than the other taxa. The climatic niche of the three species also differs, with A. ramblae occupying more arid and seasonal areas, with a higher minimum temperature in the coldest month. The estimated potential distribution for both A. brunneus and A. ramblae was most restricted in the last interglacial, becoming increasingly wider through the last glacial and the Holocene. Conclusions The A. brunneus complex diversified in the late Pleistocene, most likely in south Iberia after colonization from Morocco. Insular forms did not differentiate substantially in morphology or ecology, but A. brunneus evolved a wider tolerance to cold, which appeared to have facilitated its geographic expansion. Both A. brunneus and A. ramblae expanded their ranges during the last glacial, although they have not occupied areas beyond their LGM potential distribution except for isolated populations of A. brunneus in France and England . On the islands and possibly Tunisia secondary contact between A. brunneus and A. ramblae or A. rufulus has resulted in introgression. Our work highlights the complex dynamics of speciation and range expansions within southern areas during the last glacial cycle, and points to the often neglected role of North Africa as a source of European biodiversity.

Population proteomics has a great potential to address evolutionary and ecological questions, but its use in wild populations of non-model organisms is hampered by uncontrolled sources of variation. Here we compare the response to temperature extremes of two geographically distant populations of a diving beetle species (Agabus ramblae) using 2-D DIGE. After one week of acclimation in the laboratory under standard conditions, a third of the specimens of each population were placed at either 4 or 27°C for 12 h, with another third left as a control. We then compared the protein expression level of three replicated samples of 2-3 specimens for each treatment. Within each population, variation between replicated samples of the same treatment was always lower than variation between treatments, except for some control samples that retained a wider range of expression levels. The two populations had a similar response, without significant differences in the number of protein spots over- or under-expressed in the pairwise comparisons between treatments. We identified exemplary proteins among those differently expressed between treatments, which proved to be proteins known to be related to thermal response or stress. Overall, our results indicate that specimens collected in the wild are suitable for proteomic analyses, as the additional sources of variation were not enough to mask the consistency and reproducibility of the response to the temperature treatments.

Population proteomics has a great potential to address evolutionary and ecological questions, but its use in wild populations of non-model organisms is hampered by uncontrolled sources of variation. Here we compare the response to temperature extremes of two geographically distant populations of a diving beetle species (Agabus ramblae) using 2-D DIGE. After one week of acclimation in the laboratory under standard conditions, a third of the specimens of each population were placed at either 4 or 27 degree C for 12 h, with another third left as a control. We then compared the protein expression level of three replicated samples of 2-3 specimens for each treatment. Within each population, variation between replicated samples of the same treatment was always lower than variation between treatments, except for some control samples that retained a wider range of expression levels. The two populations had a similar response, without significant differences in the number of protein spots over- or under-expressed in the pairwise comparisons between treatments. We identified exemplary proteins among those differently expressed between treatments, which proved to be proteins known to be related to thermal response or stress. Overall, our results indicate that specimens collected in the wild are suitable for proteomic analyses, as the additional sources of variation were not enough to mask the consistency and reproducibility of the response to the temperature treatments.

Every year more than one million commercial bumblebee colonies are deployed in greenhouses worldwide for its pollination services to several commercially important crops such as tomato and different species of berries. While commercial pollinators have been an enormous benefit for the production of essential food crops and for achieving higher yields and better fruit quality at a low cost, their use is emerging also as an important threat to wild pollinators. Commercial pollinators have been linked to pathogen spillover to wild species, and its introduction outside its native area have had devastating effects on native pollinator populations. However, a more pervasive, but underappreciated threat is their potential impact on the genetic integrity of native pollinators. Here, we show clear evidence of generalized hybridization between native and introduced commercial bumblebee lineages in southern Spain. The signal of genetic introgression is widespread and already expands up to 60 km from main commercial bumblebee release areas. As pollination services demand is predicted to increase in the coming years, only a more restrictive regulation of commercial lines could mitigate their negative impacts on the genetic integrity of native pollinators and prevent the disruption of local adaptations.