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Population genetic structure, genetic diversity and sex determination in three bumblebees species in southern Sweden

Cornet, Camille (2022) BION02 20211
Degree Projects in Biology
Abstract
Bumblebees are essential pollinators of wild and cultivated plants. They have experienced global declines over the last decades mainly due to habitat loss and fragmentation caused by agricultural intensification and land use changes. Haplodiploid hymenopterans with single-locus complementary sex determination (CSD), such as bees and bumblebees, are likely to experience partly different consequences of habitat fragmentation than diploid organisms. When the population genetic diversity decreases, increasing homozygosity at the CSD locus will lead to increasing production of diploid males at the cost of (heterozygous diploid) female workers, potentially decreasing colony fitness and increasing population extinction risk. Diploid male... (More)
Bumblebees are essential pollinators of wild and cultivated plants. They have experienced global declines over the last decades mainly due to habitat loss and fragmentation caused by agricultural intensification and land use changes. Haplodiploid hymenopterans with single-locus complementary sex determination (CSD), such as bees and bumblebees, are likely to experience partly different consequences of habitat fragmentation than diploid organisms. When the population genetic diversity decreases, increasing homozygosity at the CSD locus will lead to increasing production of diploid males at the cost of (heterozygous diploid) female workers, potentially decreasing colony fitness and increasing population extinction risk. Diploid male production is an overlooked aspect of pollinator decline, and allelic diversity at the CSD locus has been proposed as a measure of population health. However, the CSD locus is not yet characterized in bumblebees, although a candidate gene has been suggested. Here, we used whole-genome sequencing of populations (pools of individuals) to evaluate the risk of increased diploid male production of bumblebees in Sweden by comparing the population genetic structure and genetic diversity of three co-occurring bumblebee species that differ in abundance and population decline (the rare Bombus muscorum, the more abundant B. sylvarum and the very common B. pascuorum). We found that the two rarer species have more structured populations than the common species, and that island and range-edge populations are particularly isolated. Isolated populations of the rarer species might therefore be most at risk of producing diploid males. However, the nucleotide diversity of B. muscorum was surprisingly high, suggesting that it is not a sufficient indicator of decline. Finally, we found no sign of balancing selection around the putative CSD locus or other genes involved in the sex determination pathway. Thus, our data do not support the candidate CSD locus proposed in the literature. Our results underline that identifying the CSD locus in bumblebees, to allow estimation of allelic diversity at that locus directly, is essential for efficient conservation management of these important pollinators. (Less)
Popular Abstract
An overlooked aspect of pollinator decline

Bumblebees are essential pollinators of many wild plants and crops but they have been experiencing drastic declines since the 1950s. One of the main causes of this decline is habitat loss and fragmentation due to agricultural intensification. Habitat loss can cause populations to decrease in size and become more isolated, increasing extinction risk.

In addition, bees (including bumblebees) have an interesting sex determination system, in which females are diploid (meaning that they have two sets of chromosomes) while males are haploid (having only one set of chromosomes, inherited from their mother). The underlying mechanism is controlled by one gene called CSD (Complementary Sex... (More)
An overlooked aspect of pollinator decline

Bumblebees are essential pollinators of many wild plants and crops but they have been experiencing drastic declines since the 1950s. One of the main causes of this decline is habitat loss and fragmentation due to agricultural intensification. Habitat loss can cause populations to decrease in size and become more isolated, increasing extinction risk.

In addition, bees (including bumblebees) have an interesting sex determination system, in which females are diploid (meaning that they have two sets of chromosomes) while males are haploid (having only one set of chromosomes, inherited from their mother). The underlying mechanism is controlled by one gene called CSD (Complementary Sex Determination). When population sizes are reduced, such as in case of habitat loss, genetic diversity at that gene decreases. This can cause diploid males to be produced instead of female workers, which is detrimental because diploid males are sterile and they don’t participate to colony growth. Diploid male production can even cause an extinction vortex. It is therefore important to consider this particular aspect of the biology of bees for efficient conservation practices.

In this project, we have used a genomic method allowing us to study many aspects of the population genetics of bumblebees in southern Sweden. The first aim was to assess which species and populations are at risk of producing diploid males by looking at genetic diversity and population isolation. We have compared three species of bumblebees that differ in their conservation status: one is rare and in decline, one is intermediate, and one is common and stable. We have also compared different types of populations, including islands and distribution margins, which are more likely to be small and isolated. The second aim was to explore the genome of these bumblebees to find the CSD gene. Indeed, it has only been characterized in honeybees but not in bumblebees. We expect natural selection to act strongly against diploid male production and therefore favour a high diversity at the CSD gene. We therefore considered those genes with particularly high diversity as CSD candidates.

Our results show that rarer and more in decline species have more isolated populations than more common species, as expected. However, genetic diversity was not lower in first than in the latter. Islands and distribution margins were also more isolated, and showed lower genetic diversity, than mainland populations (and that pattern was stronger for the rarer species than for the common ones). We conclude that isolated populations of the rarer species are the most at risk of diploid male production, while mainland populations of the most common species remain well-connected. To maintain this connectivity between populations, patches of suitable habitat should be kept within the agricultural landscape. Our search for the CSD gene in bumblebees yielded two candidate genes, but their function is presently unknown. We also showed that the candidate gene previously proposed by the literature is unlikely to be the CSD gene because it does not show the expected high diversity. Clearly, more research is needed to identify the CSD gene in bumblebees. Finding this gene would make it possible to estimate the diversity at this gene directly, which would provide a good measure of population health and extinction risk, for efficient conservation of these essential pollinators.

Master’s Degree Project in Biology, 60 credits, June 2022
Advisors: Bengt Hansson and Simon Jacobsen Ellerstrand
MEMEG, Department of Biology, Lund University (Less)
Please use this url to cite or link to this publication:
author
Cornet, Camille
supervisor
organization
course
BION02 20211
year
type
H2 - Master's Degree (Two Years)
subject
language
English
id
9102916
date added to LUP
2022-11-07 15:24:43
date last changed
2022-11-07 15:24:43
@misc{9102916,
  abstract     = {{Bumblebees are essential pollinators of wild and cultivated plants. They have experienced global declines over the last decades mainly due to habitat loss and fragmentation caused by agricultural intensification and land use changes. Haplodiploid hymenopterans with single-locus complementary sex determination (CSD), such as bees and bumblebees, are likely to experience partly different consequences of habitat fragmentation than diploid organisms. When the population genetic diversity decreases, increasing homozygosity at the CSD locus will lead to increasing production of diploid males at the cost of (heterozygous diploid) female workers, potentially decreasing colony fitness and increasing population extinction risk. Diploid male production is an overlooked aspect of pollinator decline, and allelic diversity at the CSD locus has been proposed as a measure of population health. However, the CSD locus is not yet characterized in bumblebees, although a candidate gene has been suggested. Here, we used whole-genome sequencing of populations (pools of individuals) to evaluate the risk of increased diploid male production of bumblebees in Sweden by comparing the population genetic structure and genetic diversity of three co-occurring bumblebee species that differ in abundance and population decline (the rare Bombus muscorum, the more abundant B. sylvarum and the very common B. pascuorum). We found that the two rarer species have more structured populations than the common species, and that island and range-edge populations are particularly isolated. Isolated populations of the rarer species might therefore be most at risk of producing diploid males. However, the nucleotide diversity of B. muscorum was surprisingly high, suggesting that it is not a sufficient indicator of decline. Finally, we found no sign of balancing selection around the putative CSD locus or other genes involved in the sex determination pathway. Thus, our data do not support the candidate CSD locus proposed in the literature. Our results underline that identifying the CSD locus in bumblebees, to allow estimation of allelic diversity at that locus directly, is essential for efficient conservation management of these important pollinators.}},
  author       = {{Cornet, Camille}},
  language     = {{eng}},
  note         = {{Student Paper}},
  title        = {{Population genetic structure, genetic diversity and sex determination in three bumblebees species in southern Sweden}},
  year         = {{2022}},
}