Ecological partnerships, or mutualisms, are globally widespread, sustaining agriculture and biodiversity. Mutualisms evolve through the matching of functional traits between partners, such as tongue length of pollinators and flower tube depth of plants. Long-tongued pollinators specialize on flowers with deep corolla tubes, whereas shorter-tongued pollinators generalize across tube lengths. Losses of functional guilds because of shifts in global climate may disrupt mutualisms and threaten partner species. We found that in two alpine bumble bee species, decreases in tongue length have evolved over 40 years. Co-occurring flowers have not become shallower, nor are small-flowered plants more prolific. We argue that declining floral resources because of warmer summers have favored generalist foraging, leading to a mismatch between shorter-tongued bees and the longer-tubed plants they once pollinated.
We use an extensive historical data set on bumble bee host choice collected almost 50 years ago by L. W. Macior (Melanderia 15:1-59, 1974) to examine how resource partitioning by bumble bees varies over a 2,700-m altitudinal gradient at four hierarchical scales: individual, colony, species and community. Bumble bee behavior, resource overlap between castes, and plant-bumble bee networks change with altitude in accordance with tightening temporal constraints on flowering and colony growth in alpine habitats. Individual bees were more likely to collect pollen from multiple sources at high altitude. Between-caste foraging niche overlap increased with altitude. Similarly, alpine forager networks were more highly nested than either subalpine or montane networks due to increased asymmetric specialization. However, interspecific resource partitioning showed a more complex spatial pattern with low niche overlap at intermediate altitude (subalpine) compared to montane (disturbed) and alpine (unproductive) sites. Results suggest that spatial variation in interspecific resource partitioning is driven by a shift in the behavior of long-tongued bumble bees. Long-tongued bumble bees specialized in the subalpine but generalized in montane and alpine zones. Our reanalysis of Macior's data shows that bumble bee behavior varies substantially with altitude influencing plant-bumble bee interaction networks. Results imply that pollination services to alpine host plants will change dramatically as subalpine species with unique foraging strategies move upward under global warming.
Evidence is accumulating that gene flow commonly occurs between recently-diverged species, despite the existence of barriers to gene flow in their genomes. However, we still know little about what regions of the genome become barriers to gene flow and how such barriers form. Here we compare genetic differentiation across the genomes of bumblebee species living in sympatry and allopatry to reveal the potential impact of gene flow during species divergence and uncover genetic barrier loci. We first compared the genomes of the alpine bumblebee Bombus sylvicola and a previously unidentified sister species living in sympatry in the Rocky Mountains, revealing prominent islands of elevated genetic divergence in the genome that co-localize with centromeres and regions of low recombination. This same pattern is observed between the genomes of another pair of closely-related species living in allopatry (B. bifarius and B. vancouverensis). Strikingly however, the genomic islands exhibit significantly elevated absolute divergence (dXY) in the sympatric, but not the allopatric, comparison indicating that they contain loci that have acted as barriers to historical gene flow in sympatry. Our results suggest that intrinsic barriers to gene flow between species may often accumulate in regions of low recombination and near centromeres through processes such as genetic hitchhiking, and that divergence in these regions is accentuated in the presence of gene flow.
Understanding how species with historically fragmented populations are able to persist will provide insights into which factors may be important for the maintenance of newly fragmented populations. Plants with fragmented and isolated populations, such as habitat-specialist (HS) species, are likely less attractive to pollinators and may have adaptive traits that compensate for these distributional challenges, such as larger flowers and more specialized pollination systems. If they do not have these adaptations, HS species are predicted to have lower reproductive success and be more pollen limited than widespread species. Here, I test three predictions concerning differences in reproductive traits that are known to affect attractiveness to pollinators, pollen receipt, and reproductive success, by comparing three HS species to congeneric species with broader habitat use (HT, habitat tolerators). Two of the three HS species lend partial support to the predictions that HS species have larger floral displays and more specialized pollination systems. The third HS species did not have either of these traits but did have lower relative seedset compared to its matched HT. These results provide preliminary support for a positive relationship between habitat specificity and pollination specialization, and for the role of low fecundity in contributing to range restriction of HS species.
Over the last six decades, populations of the bumblebees Bombus sylvicola and Bombus balteatus in Colorado have experienced decreases in tongue length, a trait important for plant‐pollinator mutualisms. It has been hypothesized that this observation reflects selection resulting from shifts in floral composition under climate change. Here we used morphometrics and population genomics to determine whether morphological change is ongoing, investigate the genetic basis of morphological variation, and analyse population structure in these populations. We generated a genome assembly of B. balteatus. We then analysed whole‐genome sequencing data and morphometric measurements of 580 samples of both species from seven high‐altitude localities. Out of 281 samples originally identified as B. sylvicola, 67 formed a separate genetic cluster comprising a newly‐discovered cryptic species (“incognitus”). However, an absence of genetic structure within species suggests that gene flow is common between mountains. We found a significant decrease in tongue length between bees collected between 2012–2014 and in 2017, indicating that morphological shifts are ongoing. We did not discover any genetic associations with tongue length, but a SNP related to production of a proteolytic digestive enzyme was implicated in body size variation. We identified evidence of covariance between kinship and both tongue length and body size, which is suggestive of a genetic component of these traits, although it is possible that shared environmental effects between colonies are responsible. Our results provide evidence for ongoing modification of a morphological trait important for pollination and indicate that this trait probably has a complex genetic and environmental basis.
Multiple interacting factors drive recent declines in wild and managed bees, threatening their pollination services. Widespread and intensive monitoring could lead to more effective management of wild and managed bees. However, tracking their dynamic populations is costly. We tested the effectiveness of an inexpensive, noninvasive and passive acoustic survey technique for monitoring bumble bee behavior and pollination services. First, we assessed the relationship between the first harmonic of the flight buzz (characteristic frequency) and pollinator functional traits that influence pollination success using flight cage experiments and a literature search. We analyzed passive acoustic survey data from three locations on Pennsylvania Mountain, Colorado to estimate bumble bee activity. We developed an algorithm based on Computational Auditory Scene Analysis that identified and quantified the number of buzzes recorded in each location. We then compared visual and acoustic estimates of bumble bee activity. Using pollinator exclusion experiments, we tested the power of buzz density to predict pollination services at the landscape scale for two bumble bee pollinated alpine forbs (Trifolium dasyphyllum and T. parryi). We found that the characteristic frequency was correlated with traits known to affect pollination efficacy, explaining 30–52% of variation in body size and tongue length. Buzz density was highly correlated with visual estimates of bumble bee density (r = 0.97), indicating that acoustic signals are predictive of bumble bee activity. Buzz density predicted seed set in two alpine forbs when bumble bees were permitted access to the flowers, but not when they were excluded from visiting. Our results indicate that acoustic signatures of flight can be deciphered to monitor bee activity and pollination services to bumble bee pollinated plants. We propose that applications of this technique could assist scientists and farmers in rapidly detecting and responding to bee population declines.
Pollinators at high elevations face multiple threats from climate change including heat stress, failure to phenological match advancing flower resources and competitive pressure from range-expanding species of lower elevations. We conducted long-term multi-site surveys of alpine bumble bees to determine how phenology of range-stable and range-expanding species is responding to climate change. We ask whether bumble bee responses generate mismatches with floral resources, and whether these mismatches in turn promote community disruption and potential species replacement. In alpine environments of the central Rocky Mountains, range-stable and range-expanding bumble bees exhibit phenological mismatches with flowering host plants due to earlier flowering of preferred resources under warmer spring temperatures. However, workers of range-stable species are more canalised in their foraging schedules, exploiting a relatively narrow portion of the flowering season. Specifically, range-stable species show less variance in phenology in response to temporally and spatially changing conditions than range-expanding ones. Because flowering duration drives the seasonal abundance of floral resources at the landscape scale, we hypothesize that canalisation of phenology in alpine bumble bees could reduce their access to earlier or later season flowers. Warmer conditions are decreasing abundances of range-stable alpine bumble bees above the timberline, increasing abundance of range-expanding species, and facilitating a novel and more species-diverse bumble bee community. However, this trend is not explained by greater phenological mismatch of range-stable bees. Results suggest that conversion of historic habitats for cold-adapted alpine bumble bee species into refugia for more heat-tolerant congeners is disrupting bumble bee communities at high elevations, though the precise mechanisms accounting for these changes are not yet known. If warming continues, we predict that the transient increase in diversity due to colonization by historically low-elevation species will likely give way to declines of alpine bumble bees in the central Rocky Mountains.
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