The rusty-patched bumblebee, once common in the United States, has declined from about 90% of its former range.
Photo by Jay Watson
Evolution, or more precisely change in allele frequency over time, inevitably records selection pressures on a species resulting in a genome which, when correctly read and compared to predecessors, should tell the story of changes in the species environment.
This principle is illustrated by the threatened species of bumblebee, the rusty patch bumblebee, Bombus affinis, which has recently declined by about 90% in the USA and is now considered an endangered species. If this rate of decline continues the species will probably be extinct within 20 years. This level of intense selection pressure has inevitably left its mark on the genome of the species.
On of the problems facing the species is the result of the way bees breed. The queen can normally produce two sorts of egg - a fertilised, diploid egg which will develop into a female and a haploid, unfertilised egg which will develop into a male or drone. The problem arises when there is a high level of inbreeding, due, for example, to a small population - which the bee is now facing. In that situation, the female can produce diploid males because both sets of chromosomes can be identical. Diploid males are normally sterile so reducing the breeding success of the local species.
Please explain how male bees which are normally haploid can be diploid due to inbreeding. Male bees, also known as drones, are indeed normally haploid, meaning they have one set of chromosomes (n). This is because they develop from unfertilized eggs laid by the queen bee. However, in certain cases, such as inbreeding, male bees can become diploid.A team of researchers led by Colorado State University have conducted the first range-wide genetic study of this endangered species and have shown that this reduction in population is recorded in the species genome in just this predictable way, further endangering the species. They have published their findings open access in the Journal of Insect Science and explained it in a Colorado State University News item by Jayme DeLoss:
Inbreeding occurs when individuals within a population mate with close relatives, such as siblings or cousins, leading to an increased likelihood of offspring inheriting identical copies of alleles from their parents. In the case of bees, if a diploid (2n) drone is produced due to inbreeding, it typically results from a process called "diploid drone production" or "thelytokous parthenogenesis."
Thelytokous parthenogenesis is a reproductive phenomenon where diploid female offspring are produced from unfertilized eggs. Normally, unfertilized eggs develop into haploid male bees. However, in some cases, especially in highly inbred colonies, the queen's reproductive system can malfunction, leading to the production of diploid eggs. These diploid eggs develop into diploid male bees.
Diploid male bees are usually sterile and cannot mate with queens or contribute to the colony's reproductive success. Inbreeding can lead to various genetic abnormalities and reduced fitness within the population, including the production of diploid males. Therefore, maintaining genetic diversity within bee populations is essential for their health and survival.
Tell me more about thelytokous parthenogenesis.
Thelytokous parthenogenesis is a type of asexual reproduction found in certain species where females produce female offspring from unfertilized eggs. This process bypasses the need for mating with males and the genetic recombination that occurs during sexual reproduction.
In the case of bees, thelytokous parthenogenesis is particularly notable in some species of social bees, including certain honeybees (Apis mellifera). In these species, unfertilized eggs laid by the queen bee can develop into female worker bees or, under specific circumstances, into other reproductive females known as "queens."
Thelytokous parthenogenesis in bees typically occurs through one of two mechanisms:
Thelytokous parthenogenesis can be advantageous in certain situations, such as when suitable mates are scarce or when environmental conditions are favorable for rapid population growth. However, it also comes with potential drawbacks, including reduced genetic diversity and increased susceptibility to diseases and environmental stresses.
- Automixis: In this mechanism, the egg undergoes a process similar to meiosis, during which the chromosomes duplicate and recombine within the nucleus. However, instead of separating into haploid cells as in conventional meiosis, the chromosomes remain together, resulting in a diploid egg. This diploid egg then develops into a female offspring.
- Apomixis: Apomixis involves the development of an embryo from an unfertilized egg without any intervening cell division. The egg simply develops directly into an embryo, bypassing meiosis entirely. This process can lead to the production of diploid female offspring.
In honeybees, thelytokous parthenogenesis, particularly the production of diploid female bees, can occur under specific conditions, such as in highly inbred colonies or in the presence of certain environmental cues. The resulting diploid female offspring can serve various roles within the colony, including as workers or potential replacement queens. However, diploid males are generally sterile and contribute little to the colony's reproductive success.
A team of researchers has uncovered alarming trends in the first range-wide genetic study of an endangered bee species. The study, led by Colorado State University and published in the Journal of Insect Science, will inform conservation and recovery efforts for the rusty-patched bumblebee – a species that was once common in the United States but has declined from about 90% of its historic range.Technical detail and background to the study are explained in the team's open access paper in the Journal of Insect Science:
The rusty-patched bumblebee was the first bee species to be federally listed as endangered in 2017 through the U.S. Endangered Species Act. Its numbers dropped rapidly starting in the late 1990s, likely due to a combination of pesticides, pathogens, habitat loss and degradation, and climate change.
The outlook is dire for remaining populations of this important pollinator, according to the in-depth genetic examination by a large team of collaborators, including federal and state agencies, universities, nonprofits and consultants.If that trajectory continues, this species could blink out in the next couple decades.
Assistant Professor John M Mola, lead author
Department of Forest and Rangeland Stewardship
Warner College of Natural Resources
Colorado State University, Fort Collins, CO, USA.
Even in strongholds where the bee is still found, scientists observed fewer colonies than a stable species would have and a high rate of inbreeding, which can threaten the long-term viability of a species. Of the bees sampled, 15% showed evidence of inbreeding, through the presence of what are called diploid males. In bees, males are typically haploid and have only one set of chromosomes, but when they’re inbred, they can have two sets of the same chromosomes and lack genetic diversity.
Analysis revealed three genetically distinct populations among rusty-patched bumblebees – in the upper Midwest, central Midwest and Appalachians – that will need to be handled differently for potential recovery efforts. Understanding population differentiation is key for captive rearing programs because bees from different populations might not be genetically compatible or might not survive once they’re released into the wild.When that happens, those populations essentially face a death sentence. They basically have incompatible genetic systems with other populations of the same species.
Assistant Professor John M Mola
This research is invaluable – it helps us refine healthy colony targets and shows us the importance of optimizing conservation efforts in genetically distinct areas, like the Appalachians.
Tamara A Smith, co-author
U.S. Fish and Wildlife Service,
Minnesota–Wisconsin Ecological Services Field Office, Bloomington, MN, USA.
Protecting pollinators
Pollinators, including bumblebees, are critical for food production and support many other species. Pollinators improve ecosystem health and resilience, and many crops and flowering plants depend on them.
Pollinators are critical for food production and support many other species. Restoration projects that benefit pollinators benefit other wildlife and landscape health in general.Photo by Jay Watson
There are approximately 50 species of bumblebee in North America, but there are big differences between bumblebees in the same way that there are big differences between songbirds and hawks. They’re not substitutable. Unfortunately, we’re looking at a future scenario where about one in five bumblebee species in the United States could be endangered.
Assistant Professor John M Mola
Decline of the rusty-patched bumblebee could be a harbinger of die-offs of other species that were once common.
But there is hope.
The rusty-patched bumblebee’s endangered listing has led to programs that restore habitat and the bee’s preferred plants. Pollinator-friendly home and community gardens make a difference, too, Mola said.
Additionally, restoration projects that benefit bumblebees benefit other wildlife and landscape health in general.At times, there can be doom and gloom in conservation, but there are good examples of butterfly species that have been recovered through careful conservation planning. The same thing applies with bumblebees.
Assistant Professor John M Mola
Project partners, process
Surveying the rusty-patched bumblebee across its entire U.S. range required a vast network of collaborators with proper permits to collect genetic samples from the endangered species. Sampling involved catching the bees in nets, briefly putting them on ice and clipping off a tiny bit of leg – enough to conduct the study but not so much that it would interfere with their ability to function.Michelle Boone, a University of Minnesota conservation biologist/entomologist and co-author of the study, collects rusty-patched bumblebees for genetic sampling.Photo by Tamara Smith
The project was mostly funded by the U.S. Geological Survey Science Support Partnership and the Great Lakes Restoration Initiative’s Threatened and Endangered Species Template through the U.S. Fish and Wildlife Service.Numerous partners recognized the importance of collecting these data, and we thank them for their contributions.
Tamara A Smith
The study was led by authors Mola, Smith, Ian Pearse (USGS), Michelle Boone (University of Minnesota), Elaine Evans (University of Minnesota), Mark Hepner (Metamorphic Ecological Research and Consulting), Robert Jean (Environmental Solutions and Innovations), Jade Kochanski (University of Wisconsin–Madison), Cale Nordmeyer (Minnesota Zoo), Erik Runquist (Minnesota Zoo), James Strange (Ohio State University), Jay Watson (Wisconsin Department of Natural Resources) and Jonathan Koch (U.S. Department of Agriculture).
AbstractWhere is the intelligence behind the design of a system which seems to ensure extinction when a population falls below a certain threshold unless that is the intention of it? If there is none then we must assume it was unintelligently 'designed'.
Declines in bumble bee species range and abundances are documented across multiple continents and have prompted the need for research to aid species recovery and conservation. The rusty patched bumble bee (Bombus affinis) is the first federally listed bumble bee species in North America. We conducted a range-wide population genetics study of B. affinis from across all extant conservation units to inform conservation efforts. To understand the species’ vulnerability and help establish recovery targets, we examined population structure, patterns of genetic diversity, and population differentiation. Additionally, we conducted a site-level analysis of colony abundance to inform prioritizing areas for conservation, translocation, and other recovery actions. We find substantial evidence of population structuring along an east-to-west gradient. Putative populations show evidence of isolation by distance, high inbreeding coefficients, and a range-wide male diploidy rate of ~15%. Our results suggest the Appalachians represent a genetically distinct cluster with high levels of private alleles and substantial differentiation from the rest of the extant range. Site-level analyses suggest low colony abundance estimates for B. affinis compared to similar datasets of stable, co-occurring species. These results lend genetic support to trends from observational studies, suggesting that B. affinis has undergone a recent decline and exhibit substantial spatial structure. The low colony abundances observed here suggest caution in overinterpreting the stability of populations even where B. affinis is reliably detected interannually. These results help delineate informed management units, provide context for the potential risks of translocation programs, and help set clear recovery targets for this and other threatened bumble bee species.
Introduction
Declining trends in insect abundance and diversity have increased awareness of the need to enact conservation programs aimed at preserving insect species and their habitats (Wagner 2020). Primary among these has been the recognition of declining bumble bee populations (Cameron et al. 2011, Cameron and Sadd 2020.1). Due to the higher quality of data on bumble bees compared to other insect taxa, their decline has been argued as a harbinger for other insect species more widely (Goulson and Nicholls 2016). Like other species, loss and degradation of habitat, introduced pathogens, pesticides, and climate change, as well as interactive and additive effects, factor into bumble bee declines (Cameron and Sadd 2020.1).
Informed conservation programs require genetic data to illuminate what cannot otherwise be seen from simple counts of species or measurements of morphological characteristics alone (Funk et al. 2019). The availability of genetic data for conservation programs helps us to understand the health of particular bumble bee populations, compare bumble bee population genetics to that of relatively stable species, and set target metrics for “genetic health” for listed species. This information also helps to delineate genetic management units, evaluates the risks and benefits of activities such as species reintroductions or augmentations, and aids the appropriate allocation of limited resources. Genetic information serves as a necessary first step in determining priorities and setting baselines for species-focused conservation, which sets the stage for more targeted ecological studies to hone species recovery and habitat restoration programs.
Genetic factors may play a role in bumble bee population declines, with small effective population sizes and reduced gene flow from fragmented habitats resulting in reduced viability of populations. Inbreeding and small effective population sizes may be particularly disadvantageous for bumble bees and other insects in the order Hymenoptera because, in these insects, heterozygosity determines sexual development (Zayed and Packer 2005). Thus, when AR is low, high numbers of diploid males can be produced, which increases genetic load and decreases reproductive fitness (Zayed et al. 2003). Prior studies of bumble bee population genetics in eastern North America suggest that stable species have limited evidence of population structure and relatively high colony abundance compared to declining species (Cameron et al. 2011). However, the population genetics of the first bumble bee species to be listed as federally endangered through the US Endangered Species Act (U.S. Fish and Wildlife Service 2017a, 2017.1b), the rusty patched bumble bee (Bombus affinis, Cresson), has not been studied.
Bombus affinis began declining in the late 1990s and has been lost from an estimated ~70%–90% of its historical range (Giles and Ascher 2006, Colla et al. 2012, Szymanski et al. 2016.1). The species was once broadly distributed across the northeastern United States and southeastern Canada but now is largely restricted to the upper midwestern United States and parts of the Appalachian Mountains (Fig. 1). The rusty patched bumble bee represents a broader conservation push toward understanding the causes of the decline of North American bees and finding recovery solutions.Basic population genetic information would inform the conservation of B. affinis in several meaningful ways. First, population genetics can help measure the genetic health of particular extant populations and develop target metrics for genetic health, a population attribute specifically named in the B. affinis Recovery Plan (US Fish and Wildlife Service 2021). Identifying populations that suffer from high levels of inbreeding and low levels of heterozygosity can inform management actions to increase habitat connectivity and gene flow among populations (Lozier and Zayed 2016.2). Second, understanding the overall population structure of this bee can inform the delineation of management units within larger, established conservation units (CU) (Fig. 1) and guide conservation actions within those units, as genetically disparate populations may warrant additional attention or distinct management actions. Uncovering any broad-scale population structure of this bee is critical prior to potential translocation efforts by identifying populations genetically compatible with management goals, whether those be preserving population distinctiveness or facilitating admixture (Smith et al. 2020.2). Third, genetic information is integral to counting the reproductive units (colonies) of bumble bees. This is because the reproductive unit for bumble bees is a colony, whereas the typical observation of a bumble bee is that it is a nonreproductive worker foraging outside the nest. Through genotyping, individuals observed foraging can be assigned to colonies, and then colony abundance may be estimated via genetic mark-recapture (Darvill et al. 2004, Mola et al. 2020.3). Populations at sites with very low colony abundance may be susceptible to extinction due to stochastic demographic effects and may warrant management actions to avoid major disturbances that could exacerbate those effects. All told, there is an urgent need for foundational population genetics work on B. affinis to inform recovery programs, minimize potential impacts to B. affinis, and enable future, more targeted research.Fig. 1.Map of the study area showing locations of individual specimens of Bombus affinis collected from the field in 2020 and 2021 colored by putative 100-km populations (circles) relative to the density of all US Fish and Wildlife Service B. affinis records from 2015 through 2021 (gray overlay). Background fill colors of states represent the recovery plan CU boundaries (US Fish and Wildlife Service 2021). For visual simplicity, CU 5 and states without records from 2015 to 2021 are not shown. The inset map provides regional context within the United States.
In this study, we present the results of a first-ever range-wide population genetics study with the federally endangered rusty-patched bumble bee (B. affinis). We report standard genetic measurements, based on microsatellite markers, to answer the following broad questions: (i) what is the broad-scale population structuring of B. affinis? and (ii) what are the patterns of population genetic diversity and differentiation across its extant range? Additionally, we use genetic mark-recapture analysis at the site level to answer a third question: (iii) what are the common colony abundances of B. affinis within sites, and how do they compare to other co-occurring Bombus species?
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