Evolutionary history and past climate change shape the distribution of genetic diversity in terrestrial mammals

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2020 May 22;11(1):2557.

doi: 10.1038/s41467-020-16449-5.

Spyros Theodoridis   1 ,

Damien A Fordham   2   3 ,

Stuart C Brown   3 ,

Sen Li   2   4 ,

Carsten Rahbek   2 ,

David Nogues-Bravo   5

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1 Center for Macroecology, Evolution, and Climate, GLOBE Institute, University of Copenhagen, 2100, Copenhagen Ø, Denmark. spyros.theodoridis@sund.ku.dk.

2 Center for Macroecology, Evolution, and Climate, GLOBE Institute, University of Copenhagen, 2100, Copenhagen Ø, Denmark.

3 The Environment Institute and School of Biological Sciences, University of Adelaide, 5005, Adelaide, Australia.

4 Evolutionary Genomics Section, GLOBE Institute, University of Copenhagen, 1350, Copenhagen K, Denmark.

5 Center for Macroecology, Evolution, and Climate, GLOBE Institute, University of Copenhagen, 2100, Copenhagen Ø, Denmark. dnogues@sund.ku.dk.

PMID: 32444801

PMCID: PMC7244709

DOI: 10.1038/s41467-020-16449-5

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Spyros Theodoridis  et al.

Nat Commun .

2020 .

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2020 May 22;11(1):2557.

doi: 10.1038/s41467-020-16449-5.

Authors

Spyros Theodoridis   1 ,

Damien A Fordham   2   3 ,

Stuart C Brown   3 ,

Sen Li   2   4 ,

Carsten Rahbek   2 ,

David Nogues-Bravo   5

Affiliations

1 Center for Macroecology, Evolution, and Climate, GLOBE Institute, University of Copenhagen, 2100, Copenhagen Ø, Denmark. spyros.theodoridis@sund.ku.dk.

2 Center for Macroecology, Evolution, and Climate, GLOBE Institute, University of Copenhagen, 2100, Copenhagen Ø, Denmark.

3 The Environment Institute and School of Biological Sciences, University of Adelaide, 5005, Adelaide, Australia.

4 Evolutionary Genomics Section, GLOBE Institute, University of Copenhagen, 1350, Copenhagen K, Denmark.

5 Center for Macroecology, Evolution, and Climate, GLOBE Institute, University of Copenhagen, 2100, Copenhagen Ø, Denmark. dnogues@sund.ku.dk.

PMID: 32444801

PMCID: PMC7244709

DOI: 10.1038/s41467-020-16449-5

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Abstract

Knowledge of global patterns of biodiversity, ranging from intraspecific genetic diversity (GD) to taxonomic and phylogenetic diversity, is essential for identifying and conserving the processes that shape the distribution of life. Yet, global patterns of GD and its drivers remain elusive. Here we assess existing biodiversity theories to explain and predict the global distribution of GD in terrestrial mammal assemblages. We find a strong positive covariation between GD and interspecific diversity, with evolutionary time, reflected in phylogenetic diversity, being the best predictor of GD. Moreover, we reveal the negative effect of past rapid climate change and the positive effect of inter-annual precipitation variability in shaping GD. Our models, explaining almost half of the variation in GD globally, uncover the importance of deep evolutionary history and past climate stability in accumulating and maintaining intraspecific diversity, and constitute a crucial step towards reducing the Wallacean shortfall for an important dimension of biodiversity.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1. Covariates of genetic diversity in…

Fig. 1. Covariates of genetic diversity in terrestrial mammals at two spatial scales.

Independent contribution…

Fig. 2. Correlation between biodiversity dimensions and…

Fig. 2. Correlation between biodiversity dimensions and genetic diversity at the grid cell scale.

Correlation…

Fig. 3. Predicted genetic diversity for two…

Fig. 3. Predicted genetic diversity for two mitochondrial genetic markers.

Predicted genetic diversity based on…

See this image and copyright information in PMC

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References

Cardinale BJ, et al. Biodiversity loss and its impact on humanity. Nature. 2012;486:59–67. - PubMed

Oliver TH, et al. Biodiversity and resilience of ecosystem functions. Trends Ecol. Evol. 2015;30:673–684. - PubMed

Schipper J, et al. The status of the world’s land and marine mammals: diversity, threat, and knowledge. Science. 2008;322:225–230. - PubMed

Pollock LJ, Thuiller W, Jetz W. Large conservation gains possible for global biodiversity facets. Nature. 2017;546:141–144. - PubMed

Tucker CM, et al. Assessing the utility of conserving evolutionary history. Biol. Rev. 2019;94:1740–1760. - PMC - PubMed

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Search in PubMed. Search in NLM Catalog. Add to Search. . 2020 May 22;11(1):2557. doi: 10.1038/s41467-020-16449-5. Spyros Theodoridis   1 , Damien A Fordham   2   3 , Stuart C Brown   3 , Sen Li   2   4 , Carsten Rahbek   2 , David Nogues-Bravo   5. Expand. Affiliations. 1 Center for Macroecology, Evolution, and Climate, GLOBE Institute, University of Copenhagen, 2100, Copenhagen Ø, Denmark. spyros.theodoridis@sund.ku.dk. 2 Center for Macroecology, Evolution, and Climate, GLOBE Institute, University of Copenhagen, 2100, Copenhagen Ø, Denmark. 3 The Environment Institute and School of Biological Sciences, University of Adelaide, 5005, Adelaide, Australia. 4 Evolutionary Genomics Section, GLOBE Institute, University of Copenhagen, 1350, Copenhagen K, Denmark. 5 Center for Macroecology, Evolution, and Climate, GLOBE Institute, University of Copenhagen, 2100, Copenhagen Ø, Denmark. dnogues@sund.ku.dk. PMID: 32444801. PMCID: PMC7244709. DOI: 10.1038/s41467-020-16449-5. Free PMC article. Spyros Theodoridis  et al. Nat Commun . 2020 . Free PMC article. Show details. Display options. Format. Search in PubMed. Search in NLM Catalog. Add to Search. . 2020 May 22;11(1):2557. doi: 10.1038/s41467-020-16449-5. Authors. Spyros Theodoridis   1 , Damien A Fordham   2   3 , Stuart C Brown   3 , Sen Li   2   4 , Carsten Rahbek   2 , David Nogues-Bravo   5. Affiliations. 1 Center for Macroecology, Evolution, and Climate, GLOBE Institute, University of Copenhagen, 2100, Copenhagen Ø, Denmark. spyros.theodoridis@sund.ku.dk. 2 Center for Macroecology, Evolution, and Climate, GLOBE Institute, University of Copenhagen, 2100, Copenhagen Ø, Denmark. 3 The Environment Institute and School of Biological Sciences, University of Adelaide, 5005, Adelaide, Australia. 4 Evolutionary Genomics Section, GLOBE Institute, University of Copenhagen, 1350, Copenhagen K, Denmark. 5 Center for Macroecology, Evolution, and Climate, GLOBE Institute, University of Copenhagen, 2100, Copenhagen Ø, Denmark. dnogues@sund.ku.dk. PMID: 32444801. PMCID: PMC7244709. DOI: 10.1038/s41467-020-16449-5. Cite. Display options. Format. Abstract. Knowledge of global patterns of biodiversity, ranging from intraspecific genetic diversity (GD) to taxonomic and phylogenetic diversity, is essential for identifying and conserving the processes that shape the distribution of life. Yet, global patterns of GD and its drivers remain elusive. Here we assess existing biodiversity theories to explain and predict the global distribution of GD in terrestrial mammal assemblages. We find a strong positive covariation between GD and interspecific diversity, with evolutionary time, reflected in phylogenetic diversity, being the best predictor of GD. Moreover, we reveal the negative effect of past rapid climate change and the positive effect of inter-annual precipitation variability in shaping GD. Our models, explaining almost half of the variation in GD globally, uncover the importance of deep evolutionary history and past climate stability in accumulating and maintaining intraspecific diversity, and constitute a crucial step towards reducing the Wallacean shortfall for an important dimension of biodiversity. PubMed Disclaimer. Conflict of interest statement. The authors declare no competing interests. Figures. Fig. 1. Covariates of genetic diversity in… Fig. 1. Covariates of genetic diversity in terrestrial mammals at two spatial scales. Independent contribution… Fig. 2. Correlation between biodiversity dimensions and… Fig. 2. Correlation between biodiversity dimensions and genetic diversity at the grid cell scale. Correlation… Fig. 3. Predicted genetic diversity for two… Fig. 3. Predicted genetic diversity for two mitochondrial genetic markers. Predicted genetic diversity based on… See this image and copyright information in PMC. Similar articles. Geographically divergent evolutionary and ecological legacies shape mammal biodiversity in the global tropics and subtropics. Rowan J, Beaudrot L, Franklin J, Reed KE, Smail IE, Zamora A, Kamilar JM. Rowan J, et al. Proc Natl Acad Sci U S A. 2020 Jan 21;117(3):1559-1565. doi: 10.1073/pnas.1910489116. Epub 2019 Dec 16. Proc Natl Acad Sci U S A. 2020. PMID: 31843924 Free PMC article. Two decades of climate driving the dynamics of functional and taxonomic diversity of a tropical small mammal community in western Mexico. Mason-Romo ED, Farias AA, Ceballos G. Mason-Romo ED, et al. PLoS One. 2017 Dec 11;12(12):e0189104. doi: 10.1371/journal.pone.0189104. eCollection 2017. PLoS One. 2017. PMID: 29228017 Free PMC article. Climate and species richness predict the phylogenetic structure of African mammal communities. Kamilar JM, Beaudrot L, Reed KE. Kamilar JM, et al. PLoS One. 2015 Apr 15;10(4):e0121808. doi: 10.1371/journal.pone.0121808. eCollection 2015. PLoS One. 2015. PMID: 25875361 Free PMC article. Phylogenetic diversity as a window into the evolutionary and biogeographic histories of present-day richness gradients for mammals. Davies TJ, Buckley LB. Davies TJ, et al. Philos Trans R Soc Lond B Biol Sci. 2011 Aug 27;366(1576):2414-25. doi: 10.1098/rstb.2011.0058. Philos Trans R Soc Lond B Biol Sci. 2011. PMID: 21768156 Free PMC article. Review. Environmental harshness is positively correlated with intraspecific divergence in mammals and birds. Botero CA, Dor R, McCain CM, Safran RJ. Botero CA, et al. Mol Ecol. 2014 Feb;23(2):259-68. doi: 10.1111/mec.12572. Epub 2013 Nov 27. Mol Ecol. 2014. PMID: 24283535 Review. See all similar articles. Cited by. Earth beyond six of nine planetary boundaries. Richardson K, Steffen W, Lucht W, Bendtsen J, Cornell SE, Donges JF, Druke M, Fetzer I, Bala G, von Bloh W, Feulner G, Fiedler S, Gerten D, Gleeson T, Hofmann M, Huiskamp W, Kummu M, Mohan C, Nogues-Bravo D, Petri S, Porkka M, Rahmstorf S, Schaphoff S, Thonicke K, Tobian A, Virkki V, Wang-Erlandsson L, Weber L, Rockstrom J. Richardson K, et al. Sci Adv. 2023 Sep 15;9(37):eadh2458. doi: 10.1126/sciadv.adh2458. Epub 2023 Sep 13. Sci Adv. 2023. PMID: 37703365 Free PMC article. Global determinants of insect mitochondrial genetic diversity. French CM, Bertola LD, Carnaval AC, Economo EP, Kass JM, Lohman DJ, Marske KA, Meier R, Overcast I, Rominger AJ, Staniczenko PPA, Hickerson MJ. French CM, et al. Nat Commun. 2023 Aug 29;14(1):5276. doi: 10.1038/s41467-023-40936-0. Nat Commun. 2023. PMID: 37644003 Free PMC article. Integrating biogeography and behavioral ecology to rapidly address biodiversity loss. Marske KA, Lanier HC, Siler CD, Rowe AH, Stein LR. Marske KA, et al. Proc Natl Acad Sci U S A. 2023 Apr 11;120(15):e2110866120. doi: 10.1073/pnas.2110866120. Epub 2023 Apr 5. Proc Natl Acad Sci U S A. 2023. PMID: 37018201 Free PMC article. Geographic Genetic Structure of Alectoris chukar in Turkiye: Post-LGM-Induced Hybridization and Human-Mediated Contaminations. Kaya S, Kabasakal B, Erdogan A. Kaya S, et al. Biology (Basel). 2023 Mar 3;12(3):401. doi: 10.3390/biology12030401. Biology (Basel). 2023. PMID: 36979093 Free PMC article. Population genomics reveals moderate genetic differentiation between populations of endangered Forest Musk Deer located in Shaanxi and Sichuan. Liu G, Zhang BF, Chang J, Hu XL, Li C, Xu TT, Liu SQ, Hu DF. Liu G, et al. BMC Genomics. 2022 Sep 23;23(1):668. doi: 10.1186/s12864-022-08896-9. BMC Genomics. 2022. PMID: 36138352 Free PMC article. See all "Cited by" articles. References. Cardinale BJ, et al. Biodiversity loss and its impact on humanity. Nature. 2012;486:59–67. - PubMed. Oliver TH, et al. Biodiversity and resilience of ecosystem functions. Trends Ecol. Evol. 2015;30:673–684. - PubMed. Schipper J, et al. The status of the world’s land and marine mammals: diversity, threat, and knowledge. Science. 2008;322:225–230. - PubMed. Pollock LJ, Thuiller W, Jetz W. Large conservation gains possible for global biodiversity facets. Nature. 2017;546:141–144. - PubMed. Tucker CM, et al. Assessing the utility of conserving evolutionary history. Biol. Rev. 2019;94:1740–1760. - PMC - PubMed. Publication types. Research Support, Non-U.S. Gov't Actions Search in PubMed Search in MeSH Add to Search. MeSH terms. Animals Actions Search in PubMed Search in MeSH Add to Search. Biological Evolution* Actions Search in PubMed Search in MeSH Add to Search. Climate Change* Actions Search in PubMed Search in MeSH Add to Search. Ecosystem Actions Search in PubMed Search in MeSH Add to Search. Genetic Variation* Actions Search in PubMed Search in MeSH Add to Search. Mammals / classification Actions Search in PubMed Search in MeSH Add to Search. Mammals / genetics* Actions Search in PubMed Search in MeSH Add to Search. Phylogeny Actions Search in PubMed Search in MeSH Add to Search. Related information. MedGen. PMC images. LinkOut - more resources. Full Text Sources Europe PubMed Central Nature Publishing Group PubMed Central. Medical MedlinePlus Health Information. Miscellaneous NCI CPTAC Assay Portal.