Abstract
Historic and contemporary data can shed light on a species’ conservation status and work together to address two main goals in conservation biology: (1) identifying species under extinction risk and (2) the forces shaping this process. Museomics is the study of historical DNA acquired from museum specimens that allows researchers to answer myriad questions across many taxa. Museomics is an effective way to understand how populations have been affected by human and climate factors from a historic perspective. Here, our goal is to investigate changes in wild populations of two small carpenter bee species (Ceratina calcarata and C. dupla) across a 50-year time span. We sampled museum specimens and recent collections to determine their genetic diversity, population structure, effective population size, signatures of selection, and local adaptation. Both species displayed reduced genetic diversity and effective population size through time. We identified signatures of adaptation in both species across human-altered land use and climate change scenarios. We found signatures of selection in genes related to biochemical defense, insecticide, and thermal tolerance, which are consistent with the observed increase in agricultural land use development and rising temperatures over the past 50 years. Our findings suggest that these species are facing population inbreeding, possibly attributable to human land-use change and agrochemicals in their environment. Overall, this study highlights the use of museomics to understand species declines, threats to populations, and targets for remediation.
Similar content being viewed by others
References
Alexa A, Rahnenführer J (2020) Gene set enrichment analysis with topGO. Bioconduct Improv 27:1–26
Alexander DH, Novembre J, Lange K (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19:1655–1664. https://doi.org/10.1101/gr.094052.109
Atkinson N, Robertson G, Ganetzky B (1991) A component of calcium-activated potassium channels encoded by the Drosophila slo locus. Science 253(5019):551–555. https://doi.org/10.1126/science.1857984
Ayers AC, Rehan SM (2021) Supporting bees in cities: how bees are influenced by local and landscape features. Insects 12:1–18. https://doi.org/10.3390/insects12020128
Baird NA, Etter PD, Atwood TS et al (2008) Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS ONE. https://doi.org/10.1371/journal.pone.0003376
Balkenhol N, Cushman SA, Storfer AT, Waits LP (2015) Landscape genetics: concepts, methods, applications, 1st edn. Wiley-Blackwell, London
Ballare KM, Jha S (2020) Genetic structure across urban and agricultural landscapes reveals evidence of resource specialization and philopatry in the eastern carpenter bee, Xylocopa virginica L. Evol Appl. https://doi.org/10.1111/eva.13078
Barbosa MM, Jaffé R, Carvalho CS et al (2022) Landscape influences genetic diversity but does not limit gene flow in a neotropical pollinator. Apidologie 53(4):1–16. https://doi.org/10.1007/s13592-022-00955-0
Bellard C, Bertelsmeier C, Leadley P et al (2012) Impacts of climate change on the future of biodiversity. Ecol Lett 15:365–377. https://doi.org/10.1111/j.1461-0248.2011.01736.x
Bhuller Y, Ramsingh D, Beal M et al (2021) Canadian regulatory perspective on next generation risk assessments for pest control products and industrial chemicals. Front Toxicol. https://doi.org/10.3389/ftox.2021.748406
Bi K, Linderoth T, Vanderpool D et al (2013) Unlocking the vault: next-generation museum population genomics. Mol Ecol 22:6018–6032. https://doi.org/10.1111/mec.12516
Birdshire KR, Carper AL, Briles CE (2020) Bee community response to local and landscape factors along an urban–rural gradient. Urban Ecosyst 23:689–702. https://doi.org/10.1007/s11252-020-00956-w
Burkle L, Marlin J, Knight T (2013) Plant–pollinator interactions over 120 years: loss of species, co-occurrence, and function. Science 339(6127):1611–1615. https://doi.org/10.1126/science.1232728
Burrell AS, Disotell TR, Bergey CM (2015) The use of museum specimens with high-throughput DNA sequencers. J Hum Evol 79:35–44. https://doi.org/10.1016/j.jhevol.2014.10.015
Butt S, Ramprasad P, Fenech AD (2005) Changes in the landscape of Southern Ontario Canada since 1750: impacts of European colonization. Integrated mapping assessment, pp 83–92
Cahill AE, Aiello-Lammens ME, Caitlin Fisher-Reid M et al (2013) How does climate change cause extinction? Proc R Soc B 280(1750):20121890. https://doi.org/10.1098/rspb.2012.1890
Cameron SA, Lozier JD, Strange JP et al (2011) Patterns of widespread decline in North American bumble bees. Proc Natl Acad Sci USA 108:662–667. https://doi.org/10.1073/pnas.1014743108
Chang CC, Chow CC, Tellier LCAM et al (2015) Second-generation PLINK: rising to the challenge of larger and richer datasets. GigaScience 4:7. https://doi.org/10.1186/s13742-015-0047-8
Conflitti IM, Arshad Imrit M, Morrison B et al (2022) Bees in the six: determinants of bumblebee habitat quality in urban landscapes. Ecol Evol 12:(3):e8667. https://doi.org/10.1002/ece3.8667
Crates R, Olah G, Adamski M et al (2019) Genomic impact of severe population decline in a nomadic songbird. PLoS ONE 14(10):e0223953. https://doi.org/10.1371/journal.pone.0223953
da Silva CRB, Beaman JE, Dorey JB et al (2021) Climate change and invasive species: a physiological performance comparison of invasive and endemic bees in Fiji. J Exp Biol 224(Pt 1):jeb230326. https://doi.org/10.1242/jeb.230326
Danforth BN (1999) Emergence dynamics and bet hedging in a desert bee, Perdita portalis. Proc R Soc Lond B 266:1985–1994. https://doi.org/10.1098/rspb.1999.0876
Dew RM, Rehan SM, Schwarz MP (2016) Biogeography and demography of an Australian native bee Ceratina australensis (Hymenoptera, Apidae) since the last glacial maximum. J Hymenopt Res 49:25–41. https://doi.org/10.3897/JHR.49.8066
Dew RM, Silva DP, Rehan SM (2019) Range expansion of an already widespread bee under climate change. Glob Ecol Conserv 17:e00584. https://doi.org/10.1016/j.gecco.2019.e00584
Do C, Waples RS, Peel D et al (2014) NeEstimator v2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour 14:209–214. https://doi.org/10.1111/1755-0998.12157
Dyson CJ, Piscano OL, Durham RM et al (2021) Temporal analysis of effective population size and mating system in a social wasp. J Hered 112(7):626–634. https://doi.org/10.1093/jhered/esab057
Exposito-Alonso M, Booker T, Czech L, Gillespie L, Hateley S, Kyriazis C, Lang P, Leventhal L, Nogues-Bravo D, Pagowski V, Ruffley M, Spence J, Toro, Arana S, Weiß C, Zess E (2022) Genetic diversity loss in the Anthropocene. Science 377(6613):1431–1435. https://doi.org/10.1126/science.abn5642
Fausto E, Glenn Milner O, Vladimir Nikolic O et al (2015) Historical and future climate trends in York region. Ontario Climate Consortium, Toronto, p 48
Forester BR, Lasky JR, Wagner HH, Urban DL (2018) Comparing methods for detecting multilocus adaptation with multivariate genotype–environment associations. Mol Ecol 27(9):2215–2233. https://doi.org/10.1111/mec.14584
Frankham R, Ballou J, Briscoe D (2010) Introduction to conservation genetics, 2nd edn. Cambridge University Press, Cambridge. https://doi.org/10.1017/CBO9780511809002
Franks SJ, Hoffmann AA (2012) Genetics of climate change adaptation. Annu Rev Genet 46:185–208. https://doi.org/10.1146/annurev-genet-110711-155511
Freitas FV, Branstetter MG, Griswold T, Almeida EA (2021) Partitioned gene-tree analyses and gene-based topology testing help resolve incongruence in a phylogenomic study of host-specialist bees (Apidae: Eucerinae). Mol Biol Evol 38(3):1090–1100
Garrad R, Booth DT, Furlong MJ (2016) The effect of rearing temperature on development, body size, energetics and fecundity of the diamondback moth. Bull Entomol Res 106:175–181. https://doi.org/10.1017/S000748531500098X
Gauthier J, Pajkovic M, Neuenschwander S et al (2020) Museomics identifies genetic erosion in two butterfly species across the 20th century in Finland. Mol Ecol Res 20(5):1191–1205. https://doi.org/10.1111/1755-0998.13167
Giannini TC, Acosta AL, Garófalo CA et al (2012) Pollination services at risk: bee habitats will decrease owing to climate change in Brazil. Ecol Model 244:127–131. https://doi.org/10.1016/j.ecolmodel.2012.06.035
Gordon S, Dickinson MH (2006) Role of calcium in the regulation of mechanical power in insect flight. Proc Natl Acad Sci USA 103(11):4311–4315. https://doi.org/10.1073/pnas.0510109103
Goulson D, Nicholls E, Botías C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347(6229):1255957. https://doi.org/10.1126/science.1255957
Greenleaf SS, Williams NM, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153:589–596. https://doi.org/10.1007/s00442-007-0752-9
Grixti JC, Wong LT, Cameron SA, Favret C (2009) Decline of bumble bees (Bombus) in the North American Midwest. Biol Conserv 142:75–84. https://doi.org/10.1016/j.biocon.2008.09.027
Haile J, Froese DG, MacPhee RDE et al (2009) Ancient DNA reveals late survival of mammoth and horse in interior Alaska. Proc Natl Acad Sci USA 106:22352–22357. https://doi.org/10.1073/pnas.0912510106
Harper GL, Maclean N, Goulson D (2006) Analysis of museum specimens suggests extreme genetic drift in the adonis blue butterfly (Polyommatus bellargus). Biol J Linn Soc 88(3):447–452. https://doi.org/10.1111/j.1095-8312.2006.00632.x
Harpur BA, Rehan SM (2021) Connecting social polymorphism to single nucleotide polymorphism: population genomics of the small carpenter bee, Ceratina australensis. Biol J Linn Soc 132(4):945–954. https://doi.org/10.1093/biolinnean/blab003
Hoffmann A, Griffin P, Dillon S et al (2015) A framework for incorporating evolutionary genomics into biodiversity conservation and management. Clim Change Responses 2(1):1–24. https://doi.org/10.1186/s40665-014-0009-x
Hoffmann AA, Willi Y (2008) Detecting genetic responses to environmental change. Nat Rev Genet 9:421–432. https://doi.org/10.1038/nrg2339
Holmes MW, Hammond TT, Wogan GOU et al (2016) Natural history collections as windows on evolutionary processes. Mol Ecol 25:864–881. https://doi.org/10.1111/mec.13529
Homma T, Watanabe K, Tsurumaru S et al (2006) G protein-coupled receptor for diapause hormone, an inducer of Bombyx embryonic diapause. Biochem Biophys Res Commun 344:386–393. https://doi.org/10.1016/j.bbrc.2006.03.085
Husemann M, Zachos FE, Paxton RJ, Habel JC (2016) Effective population size in ecology and evolution. Heredity (Edinb) 117:191–192. https://doi.org/10.1038/hdy.2016.75
Jackson JM, Pimsler ML, Oyen KJ et al (2020) Local adaptation across a complex bioclimatic landscape in two montane bumble bee species. Mol Ecol 29(5):920–939. https://doi.org/10.1111/mec.15376
Jha S, Kremen C (2013) Urban land use limits regional bumble bee gene flow. Mol Ecol 22:2483–2495. https://doi.org/10.1111/mec.12275
Jónsson H, Ginolhac A, Schubert M et al (2013) MapDamage2.0: fast approximate Bayesian estimates of ancient DNA damage parameters. Bioinformatics (Oxford, England) 29(13):1682–1684. https://doi.org/10.1093/bioinformatics/btt193
Jorde PE, Ryman N (2007) Unbiased estimator for genetic drift and effective population size. Genetics 177:927–935. https://doi.org/10.1534/genetics.107.075481
Karasiak N (2016) Dzetsaka Qgis classification plugin. https://doi.org/10.5281/zenodo.2552284
Kelemen EP, Rehan SM (2021) Opposing pressures of climate and land-use change on a native bee. Glob Change Biol 27:1017–1026. https://doi.org/10.1111/gcb.15468
Kennedy CM, Lonsdorf E, Neel MC et al (2013) A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems. Ecol Lett 16:584–599. https://doi.org/10.1111/ele.12082
Kent CF, Dey A, Patel H et al (2018) Conservation genomics of the declining North American bumblebee Bombus terricola reveals inbreeding and selection on immune genes. Front Genet. https://doi.org/10.3389/fgene.2018.00316
Keyser MR (2005) Calcium-activated potassium channel of the tobacco hornworm, Manduca sexta: molecular characterization and expression analysis. J Exp Biol 208(21):4167–4179. https://doi.org/10.1242/jeb.01857
Kleijn D, Winfree R, Bartomeus I et al (2015) Delivery of crop pollination services is an insufficient argument for wild pollinator conservation. Nat Commun 6:7414. https://doi.org/10.1038/ncomms8414
Kofler R, Pandey RV, Schlötterer C (2011) PoPoolation2: identifying differentiation between populations using sequencing of pooled DNA samples (Pool-Seq). Bioinform 27(24):3435–6. https://doi.org/10.1371/journal.pone.0015925
Kremen C, Williams NM, Thorp RW (2002) Crop pollination from native bees at risk from agricultural intensification. Proc Natl Acad Sci USA 99:16812–16816. https://doi.org/10.1073/pnas.262413599
Latifovic R, Zhu Z-L, Cihlar J et al (2004) Land cover mapping of North and Central America—global land cover 2000. Remote Sens Environ 89:116–127. https://doi.org/10.1016/j.rse.2003.11.002
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25:1754–1760. https://doi.org/10.1093/bioinformatics/btp324
Li H, Handsaker B, Wysoker A et al (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079. https://doi.org/10.1093/bioinformatics/btp352
Li H, Zhao X, Qiao H et al (2020) Comparative transcriptome analysis of the heat stress response in Monochamus alternatus Hope (Coleoptera: Cerambycidae). Front Physiol. https://doi.org/10.3389/fphys.2019.01568
Liu Y, Henkel J, Beaurepaire A et al (2021) Comparative genomics suggests local adaptations in the invasive small hive beetle. Ecol Evol 11:15780–15791. https://doi.org/10.1002/ece3.8242
Lonsinger RC, Adams JR, Waits LP (2018) Evaluating effective population size and genetic diversity of a declining kit fox population using contemporary and historical specimens. Ecol Evol 8(23):12011–12021. https://doi.org/10.1002/ece3.4660
Lozier JD, Cameron SA (2009) Comparative genetic analyses of historical and contemporary collections highlight contrasting demographic histories for the bumble bees Bombus pensylvanicus and B. impatiens in Illinois. Mol Ecol 18:1875–1886. https://doi.org/10.1111/j.1365-294X.2009.04160.x
MacKay PA, Knerer G (1979) Seasonal occurrence and abundance in a community of wild bees from an old field habitat in Southern Ontario. Can Entomol 111:367–376. https://doi.org/10.4039/Ent111367-3
Manjon C, Troczka BJ, Zaworra M et al (2018) Unravelling the molecular determinants of bee sensitivity to neonicotinoid insecticides. Curr Biol 28:1137–1143e5. https://doi.org/10.1016/j.cub.2018.02.045
Martin SJ, Brettell LE (2019) Deformed wing virus in honey bees and other insects. Annu Rev Virol 6(1):49–69. https://doi.org/10.1146/annurev-virology-092818-015700
Mathiasson ME, Rehan SM (2019) Status changes in the wild bees of north-eastern North America over 125 years revealed through museum specimens. Insect Conserv Divers 12:278–288. https://doi.org/10.1111/icad.12347
Matteson KC, Ascher JS, Langellotto GA (2008) Bee richness and abundance in New York City urban gardens. Ann Entomol Soc Am 101(1):140–150. https://doi.org/10.1603/0013-8746
McFrederick QS, Rehan SM (2016) Characterization of pollen and bacterial community composition in brood provisions of a small carpenter bee. Mol Ecol 25:2302–2311. https://doi.org/10.1111/mec.13608
McFrederick QS, Rehan SM (2019) Wild bee pollen usage and microbial communities covary across landscapes. Microb Ecol 77:513–522. https://doi.org/10.1007/s00248-018-1232-y
McGaughran A (2020) Effects of sample age on data quality from targeted sequencing of museum specimens: what are we capturing in time? BMC Genomics 21(1):188. https://doi.org/10.1186/s12864-020-6594-0
Meirmans PG (2020) Genodive version 3.0: easy-to‐use software for the analysis of genetic data of diploids and polyploids. Mol Ecol Res 20(4):1126–1131
Michener CD (2007) The bees of the world, 2nd edn. The Johns Hopkins University Press, Baltimore
Mikheyev AS, Tin MMY, Arora J, Seeley TD (2015) Museum samples reveal rapid evolution by wild honey bees exposed to a novel parasite. Nat Commun. https://doi.org/10.1038/ncomms8991
Nanetti A, Bortolotti L, Cilia G (2021) Pathogens spillover from honey bees to other arthropods. Pathogens 10(8):1044. https://doi.org/10.3390/pathogens10081044
NatureServe (2022) NatureServe explorer: an online encyclopedia of life [web application]. Version 7.0. http://explorer.natureserve.org
Nooten SS, Rehan SM (2019) Agricultural land use yields reduced foraging efficiency and unviable offspring in the wild bee Ceratina calcarata. Ecol Entomol 44:534–542. https://doi.org/10.1111/een.12730
Outhwaite CL, McCann P, Newbold T (2022) Agriculture and climate change are reshaping insect biodiversity worldwide. Nature 605:97–102. https://doi.org/10.1038/s41586-022-04644-x
Overgaard J, MacMillan HA (2017) The integrative physiology of insect chill tolerance. Annu Rev Physiol 79:187–208. https://doi.org/10.1146/annurev-physiol-022516-034142
Pääbo S, Poinar H, Serre D et al (2004) Genetic analyses from ancient DNA. Annu Rev Genet 38:645–679. https://doi.org/10.1146/annurev.genet.37.110801.143214
Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669. https://doi.org/10.1146/annurev.ecolsys.37.091305.110100
Pollak E (1983) A new method for estimating the effective population size from allele frequency changes. Genetics 104:531–548. https://doi.org/10.1093/genetics/104.3.531
Paxton RJ, Schäfer MO, Nazzi F et al (2022) Epidemiology of a major honey bee pathogen, deformed wing virus: potential worldwide replacement of genotype A by genotype B. Int J Parasitol Parasites Wildl 18:157–171. https://doi.org/10.1016/j.ijppaw.2022.04.013
Pope NS, Jha S (2018) Seasonal food scarcity prompts long-distance foraging by a wild social bee. Am Nat 191:45–57. https://doi.org/10.1086/694843.1
Potts SG, Biesmeijer JC, Kremen C et al (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353. https://doi.org/10.1016/j.tree.2010.01.007
Purcell S, Neale B, Todd-Brown K et al (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81:559–575. https://doi.org/10.1086/519795
Puric-Mladenovic D, Gleeson J, Nielsen G (2016) Estimating carbon storage in Southern Ontario forests at regional and stand levels. (Report number: Climate Change Research Note CCRN-12). Science and Research Branch, Ministry of Natural Resources and Forestry. https://www.researchgate.net/publication/305993420_Estimating_carbon_storage_in_southern_Ontario_forests_at_regional_and_stand_levels
Quinlan AR, Hall IM (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26:841–842. https://doi.org/10.1093/bioinformatics/btq033
Ray AM, Lopez DL, Iturralde Martinez JF et al (2020) Distribution of recently identified bee-infecting viruses in managed honey bee (Apis mellifera) populations in the USA. Apidologie 51:736–745. https://doi.org/10.1007/s13592-020-00757-2
Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17(1):230–237. https://doi.org/10.1046/j.1523-1739.2003.01236.x
Rehan SM, Richards MH (2010) Nesting biology and subsociality in Ceratina calcarata (Hymenoptera: Apidae). Can Entomol 142(1):65–74. Doi: https://doi.org/10.4039/n09-056
Reynolds S, Samuels R (1996) Physiology and biochemistry of insect moulting fluid. Adv Insect Phys 26:157–232. https://doi.org/10.1016/S0065-2806(08)60031-4
Rochette NC, Rivera-Colón AG, Catchen JM (2019) Stacks 2: analytical methods for paired-end sequencing improve RADseq-based population genomics. Mol Ecol 28:4737–4754. https://doi.org/10.1111/mec.15253
Rubens C (2019) Changes in composition and structure of a wild bee community and plant–pollinator interactions in South-Central Ontario over a forty-nine year period (Master’s thesis, University of Guelph). https://atrium.lib.uoguelph.ca/xmlui/handle/10214/17491
Saarinen EV, Austin JD, Daniels JC (2010) Genetic estimates of contemporary effective population size in an endangered butterfly indicate a possible role for genetic compensation. Evol Appl 3(1):28–39. https://doi.org/10.1111/j.1752-4571.2009.00096.x
Sawyer S, Krause J, Guschanski K et al (2012) Temporal patterns of nucleotide misincorporations and DNA fragmentation in ancient DNA. PLoS ONE 7(3):e34131. https://doi.org/10.1371/journal.pone.0034131
Segelbacher G, Cushman SA, Epperson BK et al (2010) Applications of landscape genetics in conservation biology: concepts and challenges. Conserv Genet 11:375–385. https://doi.org/10.1007/s10592-009-0044-5
Shell WA, Rehan SM (2015) Recent and rapid diversification of the small carpenter bees in eastern North America. Biol J Linn Soc 117(3):633–645. https://doi.org/10.1111/bij.12692
Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236(4803):787–792. https://doi.org/10.1126/science.3576198
Steffan-Dewenter I (2002) Landscape context affects trap-nesting bees, wasps, and their natural enemies. Ecol Entomol 27:631–637. https://doi.org/10.1046/j.1365-2311.2002.00437.x
Tehel A, Brown MJ, Paxton RJ (2016) Impact of managed honey bee viruses on wild bees. Curr Opin Virol 19:16–22. https://doi.org/10.1016/j.coviro.2016.06.006
Terhzaz S, Teets NM, Cabrero P et al (2015) Insect capa neuropeptides impact desiccation and cold tolerance. Proc Natl Acad Sci USA 112:2882–2887. https://doi.org/10.1073/pnas.1501518112
Theodorou P, Radzevičiūtė R, Kahnt B et al (2018) Genome-wide single nucleotide polymorphism scan suggests adaptation to urbanization in an important pollinator, the red-tailed bumblebee (Bombus lapidarius L.). Proc R Soc B 285(1877):20172806. https://doi.org/10.1098/rspb.2017.2806
Thomas CD, Cameron A, Green RE et al (2004) Extinction risk from climate change. Nature 427:145–148. https://doi.org/10.1038/nature02121
Thorat L, Nath BB (2018) Insects with survival kits for desiccation tolerance under extreme water deficits. Front Physiol 9:1843. https://doi.org/10.3389/fphys.2018.01843
Tsvetkov N, MacPhail VJ, Colla SR, Zayed A (2021) Conservation genomics reveals pesticide and pathogen exposure in the declining bumble bee Bombus terricola. Mol Ecol 30:4220–4230. https://doi.org/10.1111/mec.16049
vanden Broeck A, Maes D, Kelager A et al (2017) Gene flow and effective population sizes of the butterfly Maculinea alcon in a highly fragmented, anthropogenic landscape. Biol Conserv 209:89–97. https://doi.org/10.1016/j.biocon.2017.02.001
Vaudo AD, Fritz ML, López-Uribe MM (2018) Opening the door to the past: accessing phylogenetic, pathogen, and population data from museum curated bees. Insect Syst Divers 2(5):4. https://doi.org/10.1093/isd/ixy014
Vickruck JL, Richards MH (2012) Niche partitioning based on nest site selection in the small carpenter bees Ceratina mikmaqi and C. calcarata. Anim Behav 83:1083–1089. https://doi.org/10.1016/j.anbehav.2012.01.039
Wandeler P, Hoeck PEA, Keller LF (2007) Back to the future: museum specimens in population genetics. Trends Ecol Evol 22:634–642. https://doi.org/10.1016/j.tree.2007.08.017
Waples RS, Do CHI (2010) Linkage disequilibrium estimates of contemporary Ne using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evol Appl 3(3):244–262. https://doi.org/10.1111/j.1752-4571.2009.00104.x
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York. https://ggplot2.tidyverse.org
Wickham H, Averick M, Bryan J et al (2019) Welcome to the tidyverse. J Open Source Softw 4:1686. https://doi.org/10.21105/joss.01686
Wood O, Hanrahan S, Coetzee M et al (2010) Cuticle thickening associated with pyrethroid resistance in the major malaria vector Anopheles funestus. Parasites Vectors 3(1):1–7. https://doi.org/10.1186/1756-3305-3-67
Xing X, Yan M, Pang H et al (2021) Cytochrome P450s are essential for insecticide tolerance in the endoparasitoid wasp Meteorus pulchricornis (Hymenoptera: Braconidae). Insects 12(7):651. https://doi.org/10.3390/insects12070651
Acknowledgements
We thank members of the Rehan lab for providing helpful feedback on earlier versions of this manuscript. Thanks to the Raine lab (Guelph) and the Royal Ontario Museum (Toronto) for the loan of bee specimens, and Floragenex (Oregon) for library preparation and sequencing.
Funding
This study was supported by National Science Foundation (DBI-1906494 Biological Collections Postdoctoral Fellowship to EPK), Natural Sciences and Engineering Research Council of Canada (Discovery Grant, Supplement and E.W.R. Steacie Memorial Fellowship to SMR).
Author information
Authors and Affiliations
Contributions
SMR conceived and funded the study. EPK obtained specimens, conducted DNA extractions and sent material for sequencing. SNRB analyzed the data and prepared the figures. SNRB and SMR wrote the main manuscript text. All authors reviewed the manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Brasil, S.N.R., Kelemen, E.P. & Rehan, S.M. Historic DNA uncovers genetic effects of climate change and landscape alteration in two wild bee species. Conserv Genet 24, 85–98 (2023). https://doi.org/10.1007/s10592-022-01488-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-022-01488-w