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      Genetic diversity of soil invertebrates corroborates timing estimates for past collapses of the West Antarctic Ice Sheet

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          Significance

          Changes in the extent of ice sheets through evolutionary timescales have influenced the connectivity of soil invertebrate populations across the Antarctic landscape. We use genetic divergences to estimate isolation times for soil invertebrates along the Transantarctic Mountains. Four species of Collembola (Arthropoda) each showed genetically distinct populations at locations likely isolated for millions of years. Two further species were less genetically diverse although also range restricted. Our genetic data corroborate climate reconstructions and estimates of past warm periods of reduced ice and absent ice shelf in the Ross Sea region, during which time open seaways would have facilitated dispersal of Collembola, and possibly other taxa.

          Abstract

          During austral summer field seasons between 1999 and 2018, we sampled at 91 locations throughout southern Victoria Land and along the Transantarctic Mountains for six species of endemic microarthropods (Collembola), covering a latitudinal range from 76.0°S to 87.3°S. We assembled individual mitochondrial cytochrome c oxidase subunit 1 (COI) sequences ( n = 866) and found high levels of sequence divergence at both small (<10 km) and large (>600 km) spatial scales for four of the six Collembola species. We applied molecular clock estimates and assessed genetic divergences relative to the timing of past glacial cycles, including collapses of the West Antarctic Ice Sheet (WAIS). We found that genetically distinct lineages within three species have likely been isolated for at least 5.54 My to 3.52 My, while the other three species diverged more recently (<2 My). We suggest that Collembola had greater dispersal opportunities under past warmer climates, via flotation along coastal margins. Similarly increased opportunities for dispersal may occur under contemporary climate warming scenarios, which could influence the genetic structure of extant populations. As Collembola are a living record of past landscape evolution within Antarctica, these findings provide biological evidence to support geological and glaciological estimates of historical WAIS dynamics over the last ca. 5 My.

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          Most cited references52

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          A Pliocene-Pleistocene stack of 57 globally distributed benthic δ18O records

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            Revisiting the insect mitochondrial molecular clock: the mid-Aegean trench calibration.

            Phylogenetic trees in insects are frequently dated by applying a "standard" mitochondrial DNA (mtDNA) clock estimated at 2.3% My(-1), but despite its wide use reliable calibration points have been lacking. Here, we used a well-established biogeographic barrier, the mid-Aegean trench separating the western and eastern Aegean archipelago, to estimate substitution rates in tenebrionid beetles. Cytochrome oxidase I (cox1) for six codistributed genera across 28 islands (444 individuals) on both sides of the mid-Aegean trench revealed 60 independently coalescing entities delimited with a mixed Yule-coalescent model. One representative per entity was used for phylogenetic analysis of mitochondrial (cox1, 16S rRNA) and nuclear (Mp20, 28S rRNA) genes. Six nodes marked geographically congruent east-west splits whose separation was largely contemporaneous and likely to reflect the formation of the mid-Aegean trench at 9-12 Mya. Based on these "known" dates, a divergence rate of 3.54% My(-1) for the cox1 gene (2.69% when combined with the 16S rRNA gene) was obtained under the preferred partitioning scheme and substitution model selected using Bayes factors. An extensive survey suggests that discrepancies in mtDNA substitution rates in the entomological literature can be attributed to the use of different substitution models, the use of different mitochondrial gene regions, mixing of intraspecific with interspecific data, and not accounting for variance in coalescent times or postseparation gene flow. Different treatments of these factors in the literature confound estimates of mtDNA substitution rates in opposing directions and obscure lineage-specific differences in rates when comparing data from various sources.
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              DAMBE7: New and Improved Tools for Data Analysis in Molecular Biology and Evolution

              Xuhua Xia (2018)
              Abstract DAMBE is a comprehensive software package for genomic and phylogenetic data analysis on Windows, Linux, and Macintosh computers. New functions include imputing missing distances and phylogeny simultaneously (paving the way to build large phage and transposon trees), new bootstrapping/jackknifing methods for PhyPA (phylogenetics from pairwise alignments), and an improved function for fast and accurate estimation of the shape parameter of the gamma distribution for fitting rate heterogeneity over sites. Previous method corrects multiple hits for each site independently. DAMBE’s new method uses all sites simultaneously for correction. DAMBE, featuring a user-friendly graphic interface, is freely available from http://dambe.bio.uottawa.ca (last accessed, April 17, 2018).
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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc. Natl. Acad. Sci. U.S.A
                pnas
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                8 September 2020
                24 August 2020
                24 August 2020
                : 117
                : 36
                : 22293-22302
                Affiliations
                [1] aSchool of Science, University of Waikato , Hamilton 3240, New Zealand;
                [2] bCanadian High Arctic Research Station, Polar Knowledge Canada , Cambridge Bay, NU X0B 0C0, Canada;
                [3] cBritish Antarctic Survey, Natural Environment Research Council , CB3 0ET Cambridge, United Kingdom;
                [4] dDepartamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid , 28040 Madrid, Spain;
                [5] eDepartment of Biochemistry, Genetics and Microbiology, University of Pretoria , Pretoria 0002, South Africa;
                [6] fSchool of Earth Sciences, Byrd Polar and Climate Research Center, The Ohio State University , Columbus, OH 43210;
                [7] gDepartment of Biology, Brigham Young University , Provo, UT 84602;
                [8] hEvolutionary Ecology Laboratories, Brigham Young University , Provo, UT 84602;
                [9] iMonte L. Bean Museum, Brigham Young University , Provo, UT 84602;
                [10] jDepartment of Biology, Colorado State University , Fort Collins, CO 80523;
                [11] kSchool of Global Environmental Sustainability, Colorado State University , Fort Collins, CO 80523
                Author notes
                1To whom correspondence may be addressed. Email: ian.hogg@ 123456polar.gc.ca or Diana.Wall@ 123456colostate.edu .

                Contributed by Diana H. Wall, July 3, 2020 (sent for review April 29, 2020; reviewed by Brenda Hall and Bettine Jansen van Vuuren)

                Author contributions: I.D.H., B.J.A., D.H.W., and T.G.A.G. designed research; G.E.C., I.D.H., L.G.S., D.A.C., W.B.L., B.J.A., D.H.W., and T.G.A.G. performed research; G.E.C., I.D.H., and B.J.A. analyzed data; and G.E.C., I.D.H., P.C., L.G.S., D.A.C., W.B.L., B.J.A., D.H.W., and T.G.A.G. wrote the paper.

                Reviewers: B.H., University of Maine; and B.J.v.V., University of Johannesburg.

                Author information
                https://orcid.org/0000-0002-3626-7845
                https://orcid.org/0000-0002-6685-0089
                https://orcid.org/0000-0001-8497-9903
                https://orcid.org/0000-0002-4751-7475
                https://orcid.org/0000-0001-8059-861X
                https://orcid.org/0000-0002-7815-3352
                https://orcid.org/0000-0002-9466-5235
                Article
                202007925
                10.1073/pnas.2007925117
                7486705
                32839321
                74f0ffce-5623-4064-bf99-aa86e6919e4c
                Copyright © 2020 the Author(s). Published by PNAS.

                This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

                History
                Page count
                Pages: 10
                Funding
                Funded by: National Science Foundation (NSF) 100000001
                Award ID: OPP-1341736
                Award Recipient : W. Berry Lyons Award Recipient : Byron J. Adams Award Recipient : Diana H Wall
                Funded by: National Science Foundation (NSF) 100000001
                Award ID: 1637708
                Award Recipient : W. Berry Lyons Award Recipient : Byron J. Adams Award Recipient : Diana H Wall
                Funded by: Antarctica New Zealand 501100001546
                Award ID: 000
                Award Recipient : Gemma E Collins Award Recipient : Ian D Hogg
                Funded by: RCUK | NERC | British Antarctic Survey (BAS) 501100007849
                Award ID: 000
                Award Recipient : Peter Convey
                Funded by: Genome Canada (Génome Canada) 100008762
                Award ID: 000
                Award Recipient : Ian D Hogg
                Categories
                Biological Sciences
                Evolution
                Physical Sciences
                Earth, Atmospheric, and Planetary Sciences

                climate change,microarthropods,molecular clock,terrestrial biodiversity,phylogeography

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