The tragedy of the common? A comparative population genomic study of two bumblebee species

ORIGINAL ARTICLE The tragedy of the common? A comparative population genomic study of two bumblebee species

Abstract

One. Within the theoretical framework of the small population paradigm, we investigated the population genomics and parasite load of two bumblebee species across the UK and Ireland. Bombus pratorum is widespread and common throughout its range while Bombus monticola is restricted to higher altitudes and shows a more fragmented distribution.

Two. Bombus monticola showed stronger population structuring, isolation-by-distance, and a deficit of heterozygotes in the most isolated population in the south of its range (Dartmoor). Heterozygosity and inbreeding coefficients were comparable between both species, but the proportion of polymorphic sites was much greater in B. pratorum. Notably, both species have suffered significant declines in Ne over the last one hundred generations and estimates and declines for both species were of similar orders of magnitude. No pattern of increased parasite prevalence in populations of lower heterozygosity was observed. Instead, ecological and demographic factors (age, latitude, date, habitat suitability) were the main drivers of parasite prevalence.

Three. Distinct patterns of selection were observed in both species in regions involved in regulation of transcription and neurotransmission and in particular pathways targeted by neonicotinoid insecticides.

Four. Our results highlight the pressing need for monitoring to include common as well as rare species. This should not focus solely on census population counts, but include estimates of Ne. We also highlight the need for further work to establish adaptive shifts in globally important pollinator communities.

INTRODUCTION

most vulnerable to extinction. This is underpinned by the 'small population paradigm', which predicts that small populations are vulnerable to the extinction vortex. The vortex is created when populations decline to a small effective

Conservation efforts and priorities are generally focused on species that exist in small and/or declining populations since they are the size (Ne), leading to high drift load and decreasing adaptive potential. The consequent impacts on individual fitness become increasingly acute through each generation and without intervention, the interaction of demographic and genetic stochasticity can lead to extinction.

Conservation genetics has since been dominated by efforts to measure standing genetic diversity, drift, inbreeding, gene flow and effective population size. These parameters are quantified by screening neutral genetic markers since they are free from the complex potential influences of selection and are expected to behave in an evolutionarily predictable way in populations through time. Typically, such studies are restricted to single species and often in very limited geographic locations.

While this framework has led to a wealth of insightful research, criticisms have followed. First, the single rare species approach often lacks taxonomically relevant and directly comparable datasets for context, hampering the ability to correctly interpret and identify key conservation threats in wild populations. Taxonomic groups vary markedly in levels of standing genetic diversity so population genetic metrics are best interpreted in the context of comparative data from related species with similar life histories. Such comparative studies are rare, however, and while such taxonomic context may be available through other independent studies, the use of different marker sets can often make direct comparisons difficult. A single focus on rarity can also obfuscate trends in species that have historically been (and may appear to remain) relatively common. From some conservation perspectives, such species are (far more significant than those that are rare or localized since the impact of their loss or decline may be more ecologically severe. Despite the fate of the passenger pigeon, among many, and regular calls for more widespread monitoring to avoid catastrophic and rapid extirpations of more common organisms, the conservation lens remains strongly focused on rare species or populations.

Secondly, there are a number of scenarios where populations may not behave in accordance with the theoretical predictions of the SPP. Habel and Schmitt, for example, argue that highly localized 'specialist' species occurring in relatively low abundances may carry much lower genetic load due to purging or other strong selection. There is certainly good evidence that purging through selection can remove genetic load, but how effective purging will be will depend strongly on how rapid and severe declines in population sizes are (i.e., historical demography): selection driven purging processes can be overwhelmed by the strength of drift if that reduction is dramatic and fast.

Thirdly, whether genetic factors present a real extinction threat to small in situ populations has been the subject of debate since the inception of the theoretical framework. Several authors have suggested that demographic and environmental factors are more likely to drive wild populations to extinction before these genetic effects become so extreme that they directly cause extirpation. There is now compelling evidence from a wide variety of studies that the increased mutational (genetic) load created by drift and inbreeding in small populations can be linked directly to extinction risk in wild populations. Of course, these studies do not establish a general rule, but they do provide examples of where genetic factors are likely to have been important.

While there has been an emphasis on studies assessing the effects of genetic load on fitness (inbreeding depression), the parallel issue of maintaining genetic diversity to enable adaptive potential has been less controversial. Although adaptive variation is more difficult to study given our limited toolbox for identifying, functional genetic variation, clear links have been established between low genetic diversity and extinction risk.

Thus, while the ability to assess adaptive genetic diversity, particularly in non-model systems, is still in its infancy, the pressing calls for maintaining genetic diversity are unconten- tious, particularly in the face of current climate change predictions.

A final aspect of the SPP that has not been without controversy is which component of genetic diversity is most appropriate to assess. Recently, Teixeira and Huber asserted that variation at neutral genetic markers is at best only loosely linked to significant population declines and instead advocate a focus on functional genomic regions. DeWoody et al. and Kardos et al., however, present compelling evidence to the contrary and, as noted above, from a practical perspective we currently lack the sophisticated level of understanding of functional genetic diversity to enable an exclusive functional approach. There is also good evidence however, that, in some circumstances, differences in functional markers can arise between populations without notable patterns in neutral diversity being observed. Fortunately, much more comprehensive genome-wide screening has recently become accessible and affordable for population-level studies. This allows both neutral and functional markers to be screened simultaneously, and at much greater scale, significantly enhancing the resolving power of neutral markers while also giving important initial insights into variation at functional markers in non-model organisms.

Within this framework, we took a comparative, conservation genomic approach to assess paired samples from populations of two congeneric species of bumblebee across their British and Irish ranges, relating aspects of both neutral and functional genomic diversity to measures of fitness (parasite load) and habitat suitability. While data remain surprisingly limited for many species, there is strong evidence for global declines in bumblebee species along with indications that specialised species may be most vulnerable, and that declines may be phylogenetically structured. Furthermore, as eusocial, haplodiploid organisms, bumblebees are especially prone to extinction and census-based abundance estimates can be particularly misrepresentative of genetic effective population sizes. As key ecosystem service providers pollinating both crops and wildflowers, this is a group of particular conservation concern. Bumblebees also provide ideal models for testing predictions of the small population paradigm since species are variably threatened and isolated, ranging from the very rare and highly localised to those that are widespread and common.

The two congeners studied belong to the subgenus Pyrobombus, a group showing resilience to overall patterns of decline. Bombus monticola is highly localised in its distribution and included on English Nature's Programme for Recovery due to recent significant declines. In contrast, Bombus pratorum is one of the most ubiquitous species found across the UK. Several species in this subgenus have recently expanded their range including B. monticola and B. pratorum, which were first recorded in Ireland in nineteen seventy-four and nineteen forty-seven, respectively. Despite these range expansions, B. monticola has historically been restricted to areas of higher altitude across Europe, while B. pratorum represents one of the most widespread and abundant species found across a range of habitats in Europe. Neither has been the subject of landscape-scale population genetic studies to date.

Specifically, our aims were:

One. To assess and interpret genetic diversity (heterozygosity and percentage polymorphic sites), drift, inbreeding, gene flow and effective population size;

Two. To comparatively assess any associations between population genetic parameters and environmental (habitat) and biological (parasite) factors;

Three. To identify whether particular and/or consistent functional regions of the genome are under strong selection;

Four. To interpret the results in the context of the factors potentially driving declines and key conservation priorities.