Multiple Pleistocene refugia for Arctic Bell-Heather revealed with genomic analyses of modern and historic plants

Cassandra Elphinstone; Fernando Hernández; Marco Todesco; Jean Sébastien Légaré; Winnie Cheung; Paul C. Sokoloff; Annika Hofgaard; Casper T. Christiansen; Esther R. Frei; Esther Lévesque; Gergana N. Daskalova; Haydn J.D. Thomas; Isla H. Myers-Smith; Jacob A. Harris; Jeffery M. Saarela; Jeremy L. May; Joachim Obst; Julia Boike; Karin Clark; Katie MacIntosh; Katlyn R. Betway-May; Liam Case; Mats P. Björkman; Michael L. Moody; Niels Martin Schmidt; Per Molgaard; Robert G. Björk; Robert D. Hollister; Roger D. Bull; Sofie Agger; Vincent Maire; Greg H.R. Henry; Loren H. Rieseberg

doi:10.1111/jbi.14961

Multiple Pleistocene refugia for Arctic Bell-Heather revealed with genomic analyses of modern and historic plants

Cassandra Elphinstone^*, Fernando Hernández, Marco Todesco, Jean Sébastien Légaré, Winnie Cheung, Paul C. Sokoloff, Annika Hofgaard, Casper T. Christiansen, Esther R. Frei, Esther Lévesque, Gergana N. Daskalova, Haydn J.D. Thomas, Isla H. Myers-Smith, Jacob A. Harris, Jeffery M. Saarela, Jeremy L. May, Joachim Obst, Julia Boike, Karin Clark, Katie MacIntoshKatlyn R. Betway-May, Liam Case, Mats P. Björkman, Michael L. Moody, Niels Martin Schmidt, Per Molgaard, Robert G. Björk, Robert D. Hollister, Roger D. Bull, Sofie Agger, Vincent Maire, Greg H.R. Henry, Loren H. Rieseberg

^*Corresponding author for this work

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

Abstract

Aim: Arctic plants survived the Pleistocene glaciations in unglaciated refugia. The number, ages, and locations of these refugia are often unclear. We use high-resolution genomic data from present-day and Little-Ice-Age populations of Arctic Bell-Heather to re-evaluate the biogeography of this species and determine whether it had multiple independent refugia or a single refugium in Beringia. Location: Circumpolar Arctic and Coastal British Columbia (BC) alpine. Taxon: Cassiope tetragona L., subspecies saximontana and tetragona, outgroup C. mertensiana (Ericaceae). Methods: We built genotyping-by-sequencing (GBS) libraries using Cassiope tetragona tissue from 36 Arctic locations, including two ~250- to 500-year-old populations collected under glacial ice on Ellesmere Island, Canada. We assembled a de novo GBS reference to call variants. Population structure, genetic diversity and demography were inferred from PCA, ADMIXTURE, fastsimcoal2, SplitsTree, and several population genomics statistics. Results: Population structure analyses identified 4–5 clusters that align with geographic locations. Nucleotide diversity was highest in Beringia and decreased eastwards across Canada. Demographic coalescent analyses dated the following splits with Alaska: BC subspecies saximontana (5 mya), Russia (~1.4 mya), Europe (>200–600 kya), and Greenland (~60 kya). Northern Canada populations appear to have formed during the current interglacial (7–9 kya). Admixture analyses show genetic variants from Alaska appear more frequently in present-day than historic plants on Ellesmere Island. Conclusions: Population and demographic analyses support BC, Alaska, Russia, Europe and Greenland as all having had independent Pleistocene refugia. Northern Canadian populations appear to be founded during the current interglacial with genetic contributions from Alaska, Europe and Greenland. We found evidence, on Ellesmere Island, for continued recent gene flow in the last 250–500 years. These results suggest that a re-analysis of other Arctic species with shallow population structure using higher resolution genomic markers and demographic analyses may help reveal deeper structure and other circumpolar glacial refugia.

Original language	English
Journal	Journal of Biogeography
Volume	51
Issue	10
Pages (from-to)	1958-1973
Number of pages	16
ISSN	0305-0270
DOIs	https://doi.org/10.1111/jbi.14961
Publication status	Published - Oct 2024

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10.1111/jbi.14961Licence: CC BY-NC-ND

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Elphinstone, C., Hernández, F., Todesco, M., Légaré, J. S., Cheung, W., Sokoloff, P. C., Hofgaard, A., Christiansen, C. T., Frei, E. R., Lévesque, E., Daskalova, G. N., Thomas, H. J. D., Myers-Smith, I. H., Harris, J. A., Saarela, J. M., May, J. L., Obst, J., Boike, J., Clark, K., ... Rieseberg, L. H. (2024). Multiple Pleistocene refugia for Arctic Bell-Heather revealed with genomic analyses of modern and historic plants. Journal of Biogeography, 51(10), 1958-1973. https://doi.org/10.1111/jbi.14961

@article{6016a44132e4445b8b57e1c76b141415,

title = "Multiple Pleistocene refugia for Arctic Bell-Heather revealed with genomic analyses of modern and historic plants",

abstract = "Aim: Arctic plants survived the Pleistocene glaciations in unglaciated refugia. The number, ages, and locations of these refugia are often unclear. We use high-resolution genomic data from present-day and Little-Ice-Age populations of Arctic Bell-Heather to re-evaluate the biogeography of this species and determine whether it had multiple independent refugia or a single refugium in Beringia. Location: Circumpolar Arctic and Coastal British Columbia (BC) alpine. Taxon: Cassiope tetragona L., subspecies saximontana and tetragona, outgroup C. mertensiana (Ericaceae). Methods: We built genotyping-by-sequencing (GBS) libraries using Cassiope tetragona tissue from 36 Arctic locations, including two ~250- to 500-year-old populations collected under glacial ice on Ellesmere Island, Canada. We assembled a de novo GBS reference to call variants. Population structure, genetic diversity and demography were inferred from PCA, ADMIXTURE, fastsimcoal2, SplitsTree, and several population genomics statistics. Results: Population structure analyses identified 4–5 clusters that align with geographic locations. Nucleotide diversity was highest in Beringia and decreased eastwards across Canada. Demographic coalescent analyses dated the following splits with Alaska: BC subspecies saximontana (5 mya), Russia (~1.4 mya), Europe (>200–600 kya), and Greenland (~60 kya). Northern Canada populations appear to have formed during the current interglacial (7–9 kya). Admixture analyses show genetic variants from Alaska appear more frequently in present-day than historic plants on Ellesmere Island. Conclusions: Population and demographic analyses support BC, Alaska, Russia, Europe and Greenland as all having had independent Pleistocene refugia. Northern Canadian populations appear to be founded during the current interglacial with genetic contributions from Alaska, Europe and Greenland. We found evidence, on Ellesmere Island, for continued recent gene flow in the last 250–500 years. These results suggest that a re-analysis of other Arctic species with shallow population structure using higher resolution genomic markers and demographic analyses may help reveal deeper structure and other circumpolar glacial refugia.",

keywords = "ITEX, climate change, empirical population genetics, gene flow, genotyping-by-sequencing, glaciations, historic DNA, range expansion, refugia, tundra plants",

author = "Cassandra Elphinstone and Fernando Hern{\'a}ndez and Marco Todesco and L{\'e}gar{\'e}, {Jean S{\'e}bastien} and Winnie Cheung and Sokoloff, {Paul C.} and Annika Hofgaard and Christiansen, {Casper T.} and Frei, {Esther R.} and Esther L{\'e}vesque and Daskalova, {Gergana N.} and Thomas, {Haydn J.D.} and Myers-Smith, {Isla H.} and Harris, {Jacob A.} and Saarela, {Jeffery M.} and May, {Jeremy L.} and Joachim Obst and Julia Boike and Karin Clark and Katie MacIntosh and Betway-May, {Katlyn R.} and Liam Case and Bj{\"o}rkman, {Mats P.} and Moody, {Michael L.} and Schmidt, {Niels Martin} and Per Molgaard and Bj{\"o}rk, {Robert G.} and Hollister, {Robert D.} and Bull, {Roger D.} and Sofie Agger and Vincent Maire and Henry, {Greg H.R.} and Rieseberg, {Loren H.}",

year = "2024",

month = oct,

doi = "10.1111/jbi.14961",

language = "English",

volume = "51",

pages = "1958--1973",

journal = "Journal of Biogeography",

issn = "0305-0270",

publisher = "Wiley-Blackwell Publishing Ltd",

number = "10",

}

Elphinstone, C, Hernández, F, Todesco, M, Légaré, JS, Cheung, W, Sokoloff, PC, Hofgaard, A, Christiansen, CT, Frei, ER, Lévesque, E, Daskalova, GN, Thomas, HJD, Myers-Smith, IH, Harris, JA, Saarela, JM, May, JL, Obst, J, Boike, J, Clark, K, MacIntosh, K, Betway-May, KR, Case, L, Björkman, MP, Moody, ML, Schmidt, NM, Molgaard, P, Björk, RG, Hollister, RD, Bull, RD, Agger, S, Maire, V, Henry, GHR & Rieseberg, LH 2024, 'Multiple Pleistocene refugia for Arctic Bell-Heather revealed with genomic analyses of modern and historic plants', Journal of Biogeography, vol. 51, no. 10, pp. 1958-1973. https://doi.org/10.1111/jbi.14961

Multiple Pleistocene refugia for Arctic Bell-Heather revealed with genomic analyses of modern and historic plants. / Elphinstone, Cassandra; Hernández, Fernando; Todesco, Marco et al.
In: Journal of Biogeography, Vol. 51, No. 10, 10.2024, p. 1958-1973.

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

TY - JOUR

T1 - Multiple Pleistocene refugia for Arctic Bell-Heather revealed with genomic analyses of modern and historic plants

AU - Elphinstone, Cassandra

AU - Hernández, Fernando

AU - Todesco, Marco

AU - Légaré, Jean Sébastien

AU - Cheung, Winnie

AU - Sokoloff, Paul C.

AU - Hofgaard, Annika

AU - Christiansen, Casper T.

AU - Frei, Esther R.

AU - Lévesque, Esther

AU - Daskalova, Gergana N.

AU - Thomas, Haydn J.D.

AU - Myers-Smith, Isla H.

AU - Harris, Jacob A.

AU - Saarela, Jeffery M.

AU - May, Jeremy L.

AU - Obst, Joachim

AU - Boike, Julia

AU - Clark, Karin

AU - MacIntosh, Katie

AU - Betway-May, Katlyn R.

AU - Case, Liam

AU - Björkman, Mats P.

AU - Moody, Michael L.

AU - Schmidt, Niels Martin

AU - Molgaard, Per

AU - Björk, Robert G.

AU - Hollister, Robert D.

AU - Bull, Roger D.

AU - Agger, Sofie

AU - Maire, Vincent

AU - Henry, Greg H.R.

AU - Rieseberg, Loren H.

PY - 2024/10

Y1 - 2024/10

N2 - Aim: Arctic plants survived the Pleistocene glaciations in unglaciated refugia. The number, ages, and locations of these refugia are often unclear. We use high-resolution genomic data from present-day and Little-Ice-Age populations of Arctic Bell-Heather to re-evaluate the biogeography of this species and determine whether it had multiple independent refugia or a single refugium in Beringia. Location: Circumpolar Arctic and Coastal British Columbia (BC) alpine. Taxon: Cassiope tetragona L., subspecies saximontana and tetragona, outgroup C. mertensiana (Ericaceae). Methods: We built genotyping-by-sequencing (GBS) libraries using Cassiope tetragona tissue from 36 Arctic locations, including two ~250- to 500-year-old populations collected under glacial ice on Ellesmere Island, Canada. We assembled a de novo GBS reference to call variants. Population structure, genetic diversity and demography were inferred from PCA, ADMIXTURE, fastsimcoal2, SplitsTree, and several population genomics statistics. Results: Population structure analyses identified 4–5 clusters that align with geographic locations. Nucleotide diversity was highest in Beringia and decreased eastwards across Canada. Demographic coalescent analyses dated the following splits with Alaska: BC subspecies saximontana (5 mya), Russia (~1.4 mya), Europe (>200–600 kya), and Greenland (~60 kya). Northern Canada populations appear to have formed during the current interglacial (7–9 kya). Admixture analyses show genetic variants from Alaska appear more frequently in present-day than historic plants on Ellesmere Island. Conclusions: Population and demographic analyses support BC, Alaska, Russia, Europe and Greenland as all having had independent Pleistocene refugia. Northern Canadian populations appear to be founded during the current interglacial with genetic contributions from Alaska, Europe and Greenland. We found evidence, on Ellesmere Island, for continued recent gene flow in the last 250–500 years. These results suggest that a re-analysis of other Arctic species with shallow population structure using higher resolution genomic markers and demographic analyses may help reveal deeper structure and other circumpolar glacial refugia.

AB - Aim: Arctic plants survived the Pleistocene glaciations in unglaciated refugia. The number, ages, and locations of these refugia are often unclear. We use high-resolution genomic data from present-day and Little-Ice-Age populations of Arctic Bell-Heather to re-evaluate the biogeography of this species and determine whether it had multiple independent refugia or a single refugium in Beringia. Location: Circumpolar Arctic and Coastal British Columbia (BC) alpine. Taxon: Cassiope tetragona L., subspecies saximontana and tetragona, outgroup C. mertensiana (Ericaceae). Methods: We built genotyping-by-sequencing (GBS) libraries using Cassiope tetragona tissue from 36 Arctic locations, including two ~250- to 500-year-old populations collected under glacial ice on Ellesmere Island, Canada. We assembled a de novo GBS reference to call variants. Population structure, genetic diversity and demography were inferred from PCA, ADMIXTURE, fastsimcoal2, SplitsTree, and several population genomics statistics. Results: Population structure analyses identified 4–5 clusters that align with geographic locations. Nucleotide diversity was highest in Beringia and decreased eastwards across Canada. Demographic coalescent analyses dated the following splits with Alaska: BC subspecies saximontana (5 mya), Russia (~1.4 mya), Europe (>200–600 kya), and Greenland (~60 kya). Northern Canada populations appear to have formed during the current interglacial (7–9 kya). Admixture analyses show genetic variants from Alaska appear more frequently in present-day than historic plants on Ellesmere Island. Conclusions: Population and demographic analyses support BC, Alaska, Russia, Europe and Greenland as all having had independent Pleistocene refugia. Northern Canadian populations appear to be founded during the current interglacial with genetic contributions from Alaska, Europe and Greenland. We found evidence, on Ellesmere Island, for continued recent gene flow in the last 250–500 years. These results suggest that a re-analysis of other Arctic species with shallow population structure using higher resolution genomic markers and demographic analyses may help reveal deeper structure and other circumpolar glacial refugia.

KW - ITEX

KW - climate change

KW - empirical population genetics

KW - gene flow

KW - genotyping-by-sequencing

KW - glaciations

KW - historic DNA

KW - range expansion

KW - refugia

KW - tundra plants

UR - http://www.scopus.com/inward/record.url?scp=85195409898&partnerID=8YFLogxK

U2 - 10.1111/jbi.14961

DO - 10.1111/jbi.14961

M3 - Journal article

SN - 0305-0270

VL - 51

SP - 1958

EP - 1973

JO - Journal of Biogeography

JF - Journal of Biogeography

IS - 10

ER -

Multiple Pleistocene refugia for Arctic Bell-Heather revealed with genomic analyses of modern and historic plants

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Multiple Pleistocene refugia for Arctic Bell-Heather revealed with genomic analyses of modern and historic plants

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