Climate and genetic diversity change in mammals during the Late Quaternary

Conservation decisions and future scenarios are in need of past baselines on climate change impacts in biodiversity. Although we know that climate change has contributed to diversity shifts in some mammals1,2,3,4,5,6,7, previous research often assumed that climate change is invariable across species’ ranges. We are therefore still ignorant of the true rates of climate change experienced by species assemblages over the last millennia, their impacts on intraspecific diversity, and how they compare to future climate change projections. Here, we use more than 9,000 Late Quaternary records, including fossils and ancient and modern DNA sequences, millennial-scale paleoclimatic reconstructions over the last 50,000 years and future climate change projections to document rates of climate change velocity and dynamics in genetic diversity experienced by an assemblage of 16 extinct and extant Holarctic mammal species. Extinct megafauna experienced velocities more than 15 times faster than the extant species, up to 15.2 km per decade. Notably, extant large-bodied grazers lost almost a 65% of their pool of genetic diversity since the Late Pleistocene, which indicates reduced ability to adapt to on-going global change. Additionally, mammal species experienced overall climate change velocities slower than that projected for the end of the 21st century but punctuated by comparable fast climate change episodes. Our results provide baselines on the impacts of ongoing and future climate change on the diversity of mammal species.

[1]  Joshua L. Payne,et al.  Cryptic genetic variation accelerates evolution by opening access to diverse adaptive peaks , 2019, Science.

[2]  J. Watson,et al.  Climate Velocity Can Inform Conservation in a Warming World. , 2018, Trends in ecology & evolution.

[3]  G. Zazula,et al.  Megafaunal isotopes reveal role of increased moisture on rangeland during late Pleistocene extinctions , 2017, Nature Ecology &Evolution.

[4]  P. D. Polly,et al.  Merging paleobiology with conservation biology to guide the future of terrestrial ecosystems , 2017, Science.

[5]  D. Faith,et al.  Understanding and monitoring the consequences of human impacts on intraspecific variation , 2016, Evolutionary applications.

[6]  Sen Li,et al.  An Anthropocene map of genetic diversity , 2016, Science.

[7]  S. Dobrowski,et al.  Climate change velocity underestimates climate change exposure in mountainous regions , 2016, Nature Communications.

[8]  L. Orlando,et al.  Evolutionary Patterns and Processes: Lessons from Ancient DNA , 2016, Systematic biology.

[9]  Antoine Guisan,et al.  The regional species richness and genetic diversity of Arctic vegetation reflect both past glaciations and current climate , 2016 .

[10]  Owen L. Petchey,et al.  Biodiversity and Resilience of Ecosystem Functions. , 2015, Trends in ecology & evolution.

[11]  Konrad A Hughen,et al.  Abrupt warming events drove Late Pleistocene Holarctic megafaunal turnover , 2015, Science.

[12]  Swapan Mallick,et al.  Complete Genomes Reveal Signatures of Demographic and Genetic Declines in the Woolly Mammoth , 2015, Current Biology.

[13]  D. Storch,et al.  Differential effects of temperature change and human impact on European Late Quaternary mammalian extinctions , 2015, Global change biology.

[14]  L. Orlando,et al.  Using Ancient DNA to Understand Evolutionary and Ecological Processes , 2014 .

[15]  L. Duret,et al.  Comparative population genomics in animals uncovers the determinants of genetic diversity , 2014, Nature.

[16]  R. A. Garcia,et al.  Multiple Dimensions of Climate Change and Their Implications for Biodiversity , 2014, Science.

[17]  P. Taberlet,et al.  Fifty Thousand Years of Arctic Vegetation and Megafaunal Diet 1 Reconstruction of Arctic Vegetation from Permafrost Samples 121 , 2022 .

[18]  Helen M. Regan,et al.  Bioclimatic velocity: the pace of species exposure to climate change , 2014 .

[19]  Mikael Brandström,et al.  Holarctic genetic structure and range dynamics in the woolly mammoth , 2013, Proceedings of the Royal Society B: Biological Sciences.

[20]  Christopher Bronk Ramsey,et al.  Recent and Planned Developments of the Program OxCal , 2013, Radiocarbon.

[21]  Neo D. Martinez,et al.  Approaching a state shift in Earth’s biosphere , 2012, Nature.

[22]  Shane S. Sturrock,et al.  Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data , 2012, Bioinform..

[23]  James Haile,et al.  Species-specific responses of Late Quaternary megafauna to climate and humans , 2011, Nature.

[24]  R. G. Davies,et al.  The Influence of Late Quaternary Climate-Change Velocity on Species Endemism , 2011, Science.

[25]  C. Marshall,et al.  Has the Earth’s sixth mass extinction already arrived? , 2011, Nature.

[26]  A. Hoffmann,et al.  Climate change and evolutionary adaptation , 2011, Nature.

[27]  P. Friedlingstein,et al.  Late Holocene methane rise caused by orbitally controlled increase in tropical sources , 2011, Nature.

[28]  M. Navascués,et al.  Combining contemporary and ancient DNA in population genetic and phylogeographical studies , 2010, Molecular ecology resources.

[29]  J. Blois,et al.  Small mammal diversity loss in response to late-Pleistocene climatic change , 2010, Nature.

[30]  Erik Axelsson,et al.  Ancient DNA analyses exclude humans as the driving force behind late Pleistocene musk ox (Ovibos moschatus) population dynamics , 2010, Proceedings of the National Academy of Sciences.

[31]  J. Stewart,et al.  Refugia revisited: individualistic responses of species in space and time , 2010, Proceedings of the Royal Society B: Biological Sciences.

[32]  C. Field,et al.  The velocity of climate change , 2009, Nature.

[33]  Ludovic Orlando,et al.  Using Classical Population Genetics Tools with Heterochroneous Data: Time Matters! , 2009, PloS one.

[34]  S. Ho,et al.  Accommodating the effect of ancient DNA damage on inferences of demographic histories. , 2009, Molecular biology and evolution.

[35]  Bruce D. Patterson,et al.  The Status of the World's Land and Marine Mammals: Diversity, Threat, and Knowledge , 2008, Science.

[36]  Erik Axelsson,et al.  The effect of ancient DNA damage on inferences of demographic histories. , 2008, Molecular biology and evolution.

[37]  Marie-Louise Siggaard-Andersen,et al.  High-Resolution Greenland Ice Core Data Show Abrupt Climate Change Happens in Few Years , 2008, Science.

[38]  Joaquín Hortal,et al.  Climate Change, Humans, and the Extinction of the Woolly Mammoth , 2008, PLoS biology.

[39]  A. Barnosky,et al.  Late Quaternary Extinctions: State of the Debate , 2006 .

[40]  M. Vellend,et al.  Connections between species diversity and genetic diversity , 2005 .

[41]  R. Frankham,et al.  Most species are not driven to extinction before genetic factors impact them. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[42]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[43]  John F. B. Mitchell,et al.  The simulation of SST, sea ice extents and ocean heat transports in a version of the Hadley Centre coupled model without flux adjustments , 2000 .

[44]  H. Gregory McDonald,et al.  Spatial Response of Mammals to Late Quaternary Environmental Fluctuations , 1996, Science.

[45]  M. Nei,et al.  Mathematical model for studying genetic variation in terms of restriction endonucleases. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[46]  C. Buck,et al.  IntCal13 and Marine13 Radiocarbon Age Calibration Curves 0–50,000 Years cal BP , 2013, Radiocarbon.

[47]  Peter Dalgaard,et al.  R Development Core Team (2010): R: A language and environment for statistical computing , 2010 .

[48]  Paul J. Valdes,et al.  High-latitude climate sensitivity to ice-sheet forcing over the last 120 kyr , 2010 .

[49]  Christopher Bronk Ramsey,et al.  BAYESIAN ANALYSIS OF RADIOCARBON DATES , 2009 .

[50]  T. H. Andel The Climate and Landscape of the Middle Part of the Weichselian Glaciation in Europe: The Stage 3 Project , 2002 .

[51]  M. Nei,et al.  DNA polymorphism detectable by restriction endonucleases. , 1981, Genetics.