Selection despite low genetic diversity and high gene flow in a rapid island invasion of the bumblebee, Bombus terrestris.

Invasive species are predicted to adjust their morphological, physiological and life-history traits to adapt to their non-native environments. Although a loss of genetic variation during invasion may restrict local adaptation, introduced species often thrive in novel environments. Despite being founded by just a few individuals, Bombus terrestris (Hymenoptera: Apidae) has in less than 30 years successfully spread across the island of Tasmania (Australia), becoming abundant and competitive with native pollinators. We use RADseq to investigate what neutral and adaptive genetic processes associated with environmental and morphological variation allow B. terrestris to thrive as an invasive species in Tasmania. Given the widespread abundance of B. terrestris, we expected little genetic structure across Tasmania and weak signatures of environmental and morphological selection. We found high gene flow with low genetic diversity, although with significant isolation-by-distance and spatial variation in effective migration rates. Restricted migration was evident across the mid-central region of Tasmania, corresponding to higher elevations, pastural land, low wind speeds and low precipitation seasonality. Tajima's D indicated a recent population expansion extending from the south to the north of the island. Selection signatures were found for loci in relation to precipitation, wind speed and wing loading. Candidate loci were annotated to genes with functions related to cuticle water retention and insect flight muscle stability. Understanding how a genetically impoverished invasive bumblebee has rapidly adapted to a novel island environment provides further understanding about the evolutionary processes that determine successful insect invasions, and the potential for invasive hymenopteran pollinators to spread globally.

Morphological Variation in Bumblebees (Bombus terrestris) (Hymenoptera: Apidae) After Three Decades of an Island Invasion.

Introduced social insects can be highly invasive outside of their native range. Around the world, the introduction and establishment of the eusocial bumblebee Bombus terrestris (L. 1758) (Hymenoptera: Apidae) has negatively impacted native pollinators and ecosystems. Understanding how morphological variation is linked to environmental variation across invasive ranges can indicate how rapidly species may be diverging or adapting across novel ranges and may assist with predicting future establishment and spread. Here we investigate whether B. terrestris shows morphological variation related to environmental variation across the island of Tasmania (Australia) where it was introduced three decades ago. We collected 169 workers from 16 sites across Tasmania and related relative abundance and morphology to landscape-wide climate, land use, and vegetation structure. We found weak morphological divergence related to environmental conditions across Tasmania. Body size of B. terrestris was positively associated with the percentage of urban land cover, a relationship largely driven by a single site, possibly reflecting high resource availability in urban areas. Proboscis length showed a significant negative relationship with the percentage of pasture. Wing loading and local abundance were not related to the environmental conditions within sites. Our results reflect the highly adaptable nature of B. terrestris and its ability to thrive in different environments, which may have facilitated the bumblebee's successful invasion across Tasmania.

Genomic divergence and a lack of recent introgression between commercial and wild bumblebees (Bombus terrestris).

The global movement of bees for agricultural pollination services can affect local pollinator populations via hybridization. When commercial bumblebees are of the same species but of different geographic origin, intraspecific hybridization may result in beneficial integration of new genetic variation, or alternatively may disrupt locally adapted gene complexes. However, neither the existence nor the extent of genomic introgression and evolutionary divergence between wild and commercial bumblebees is fully understood. We obtained whole-genome sequencing data from wild and commercial Bombus terrestris collected from sites in Southern Sweden with and without long-term use of commercially imported B. terrestris. We search for evidence of introgression, dispersal and genome-wide differentiation in a comparative genomic analysis of wild and commercial bumblebees. Commercial B. terrestris were found in natural environments near sites where commercial bumblebees were used, as well as drifting wild B. terrestris in commercial bumblebee colonies. However, we found no evidence for widespread, recent genomic introgression of commercial B. terrestris into local wild conspecific populations. We found that wild B. terrestris had significantly higher nucleotide diversity (Nei's pi, π), while the number of segregating sites (Watterson's theta, θw) was higher in commercial B. terrestris. A highly divergent region on chromosome 11 was identified in commercial B. terrestris and found to be enriched with structural variants. The genes present in this region are involved in flight muscle contraction and structure and pathogen immune response, providing evidence for differing evolutionary processes operating in wild and commercial B. terrestris. We did not find evidence for recent introgression, suggesting that co-occurring commercial B. terrestris have not disrupted evolutionary processes in wild B. terrestris populations.

Temporal patterns in ecosystem services research: A review and three recommendations.

Temporal aspects of ecosystem services have gained surprisingly little attention given that ecosystem service flows are not static but change over time. We present the first systematic review to describe and establish how studies have assessed temporal patterns in supply and demand of ecosystem services. 295 studies, 2% of all studies engaging with the ecosystem service concept, considered changes in ecosystem services over time. Changes were mainly characterised as monotonic and linear (81%), rather than non-linear or through system shocks. Further, a lack of focus of changing ecosystem service demand (rather than supply) hampers our understanding of the temporal patterns of ecosystem services provision and use. Future studies on changes in ecosystem services over time should (1) more explicitly study temporal patterns, (2) analyse trade-offs and synergies between services over time, and (3) integrate changes in supply and demand and involve and empower stakeholders in temporal ecosystem services research.

Rodents, not birds, dominate predation-related ecosystem services and disservices in vertebrate communities of agricultural landscapes.

To understand the relationship between conservation measures and agricultural yields, we need to know the contributions of organisms to both ecosystem services and disservices. We studied the activity and contribution of birds and mammals to intermediate ecosystem services (predation of weed seeds or invertebrate pests) and disservices (predation of crop seeds or beneficial invertebrates) in southern Sweden between June and November 2016. We measured seed and invertebrate predation rates using trays placed in front of 32 wildlife cameras in 16 cereal fields with a local habitat contrast (8 fields adjacent to another crop field and 8 fields adjacent to a semi-natural grassland) and along a landscape heterogeneity gradient (amount of semi-natural grassland). Both activity and predation were dominated by small mammals (mainly rodents), yet only a few species contributed to predation services and disservices according to camera records. Small mammal activity and predation varied considerably over time. Small mammal activity was significantly higher at trays with crop seeds or beneficial invertebrate prey compared to trays with pest prey, and crop seed predation by small mammals was significantly higher than weed seed predation. In contrast, bird activity and predation did not differ significantly between resource types, but varied over time depending on the habitat contrast. Predation of animal prey by birds was highest after cereal harvest, independent of habitat contrast. Our study highlights that birds and in particular rodents provide important intermediate ecosystem services, but also disservices, which fluctuate strongly in intensity over time.

Predation-mediated ecosystem services and disservices in agricultural landscapes.

Ecological intensification may reduce environmental externalities of agriculture by harnessing biodiversity to benefit regulating ecosystem services. However, to propose management options for the production of such services, there is a need to understand the spatiotemporal dynamics of net effects between ecosystem services and disservices provided by wild organisms across taxonomic groups in relation to habitat and landscape management. We studied the contribution of predatory vertebrates and invertebrates (including both carnivores and seed herbivores) to regulating ecosystem services and disservices in 16 cereal fields in response to a local habitat contrast and a landscape complexity gradient. From May to November 2016, we provided weed (predation reflects an ecosystem service) and crop (predation reflects a disservice) seeds, as well as pest (predation reflects an ecosystem service) and beneficial (predation reflects a disservice) invertebrate prey to predators. Seed predation was dominated by vertebrates, while vertebrates and invertebrates contributed equally to predation of animal prey. Before harvest, predation steadily increased from very low levels in May to high levels in July independent of the resource type. After harvest, ecosystem services declined more rapidly than disservices. The presence of adjacent seminatural grasslands promoted crop seed predation, but reduced pest prey predation. Predation on beneficial prey decreased with increasing proportions of seminatural grassland in the landscape. Predatory vertebrates and invertebrates provide important ecosystem services due to the consumption of pests. However, beneficial invertebrates and crop seeds were often consumed to a similar or even higher extent than harmful invertebrates or weed seeds. Our results therefore raise concerns that management options aimed at enhancing service providers may simultaneously increase levels of disservices. By considering positive and negative effects simultaneously, this study addresses an important knowledge gap and highlights the importance of interactions between local management, landscape composition, and service and disservice provision across taxa and over time. Considering trade-offs between ecosystem services and disservices when evaluating the net effects of biodiversity conservation measures on ecosystem service provision is crucial. Future agri-environment schemes that offer payments for seminatural habitats may need to provide higher compensation for farmers in cases where net effects are likely to be negative.