Poleward bound: biological impacts of Southern Hemisphere glaciation
2012; Elsevier BV; Volume: 27; Issue: 8 Linguagem: Inglês
10.1016/j.tree.2012.04.011
ISSN1872-8383
AutoresCeridwen I. Fraser, Raisa Nikula, Daniel E. Ruzzante, Jonathan M. Waters,
Tópico(s)Marine Biology and Ecology Research
ResumoPostglacial recolonisation patterns are well documented for the Northern Hemisphere biota, but comparable processes in the Southern Hemisphere have only recently been examined. In the largely terrestrial Northern Hemisphere, recession of ice after the Last Glacial Maximum (LGM) allowed various taxa, including slow-moving terrestrial species, to migrate poleward. By contrast, the Southern Hemisphere polar region is completely ringed by ocean, and recolonisation of Antarctica and the sub-Antarctic islands has thus presented considerable challenges. Although a few highly dispersive marine species have been able to recolonise postglacially, most surviving high-latitude taxa appear to have persisted throughout glacial maxima in local refugia. These contrasting patterns highlight the importance of habitat continuity in facilitating biological range shifts in response to climate change. Postglacial recolonisation patterns are well documented for the Northern Hemisphere biota, but comparable processes in the Southern Hemisphere have only recently been examined. In the largely terrestrial Northern Hemisphere, recession of ice after the Last Glacial Maximum (LGM) allowed various taxa, including slow-moving terrestrial species, to migrate poleward. By contrast, the Southern Hemisphere polar region is completely ringed by ocean, and recolonisation of Antarctica and the sub-Antarctic islands has thus presented considerable challenges. Although a few highly dispersive marine species have been able to recolonise postglacially, most surviving high-latitude taxa appear to have persisted throughout glacial maxima in local refugia. These contrasting patterns highlight the importance of habitat continuity in facilitating biological range shifts in response to climate change. The geographic characteristics of the polar regions of the Southern and Northern Hemispheres are strikingly different from one another. The North Pole falls in an ocean ringed by continental land, whereas the South Pole sits in the middle of a continent surrounded by ocean (Box 1). Such contrasting environments present considerably different challenges to the associated high-latitude biota.Box 1General patterns of biological response to Quaternary climate change cycles in the Northern and Southern Hemisphere high latitudesAlthough many Southern Hemisphere taxa were presumably forced to lower latitudes, or driven locally extinct, with the onset of Quaternary glaciations, few appear to have recolonised the high latitudes postglacially. The oceanic fronts and strong circumpolar currents encircling Antarctica can act as effective barriers to latitudinal biological dispersal [26Wilson N.G. et al.Ocean barriers and glaciation: evidence for explosive radiation of mitochondrial lineages in the Antarctic sea slug Doris kerguelenensis (Mollusca, Nudibranchia).Mol. Ecol. 2009; 18: 965-984Crossref PubMed Scopus (136) Google Scholar, 27Janosik A. et al.Evolutionary history of Southern Ocean Odontaster sea star species (Odontasteridae; Asteroidea).Polar Biol. 2011; 34: 575-586Crossref Scopus (51) Google Scholar, 53González-Wevar C.A. et al.Molecular phylogeny and historical biogeography of Nacella (Patellogastropoda: Nacellidae) in the Southern Ocean.Mol. Phylogenet. Evol. 2010; 56: 115-124Crossref PubMed Scopus (69) Google Scholar, 91Wilson N. et al.Multiple lineages and absence of panmixia in the 'circumpolar' crinoid Promachocrinus kerguelensis from the Atlantic sector of Antarctica.Mar. Biol. 2007; 152: 895-904Crossref Scopus (114) Google Scholar, 92Diaz A. et al.Evolutionary pathways among shallow and deep-sea echinoids of the genus Sterechinus in the Southern Ocean.Deep Sea Res. Part II: Top. Stud. Oceanogr. 2011; 58: 205-211Crossref Scopus (66) Google Scholar], and have probably prevented many taxa from dispersing to the Antarctic and sub-Antarctic regions during warm interglacial periods, with some exceptions [93Aronson R.B. et al.Climate change and invasibility of the Antarctic benthos.Annu. Rev. Ecol. Evol. S. 2007; 38: 129-154Crossref Scopus (216) Google Scholar, 94Clarke A. et al.How isolated is Antarctica?.Trends Ecol. Evol. 2005; 20: 1-3Abstract Full Text Full Text PDF PubMed Scopus (215) Google Scholar]. Most taxa present in these southern regions are inferred to have persisted in local refugia throughout recent glaciations. By contrast, Northern Hemisphere taxa, both marine and terrestrial, highly mobile and sedentary, have experienced more dynamic histories, with major northward range shifts during interglacial periods in the absence of strong oceanographic barriers comparable to the southern ACC, APF and STC (although, in some cases, mountain ranges have limited their postglacial dispersal [1Hewitt G. The genetic legacy of the Quaternary ice ages.Nature. 2000; 405: 907-913Crossref PubMed Scopus (5120) Google Scholar]) (Figure I). Although many Southern Hemisphere taxa were presumably forced to lower latitudes, or driven locally extinct, with the onset of Quaternary glaciations, few appear to have recolonised the high latitudes postglacially. The oceanic fronts and strong circumpolar currents encircling Antarctica can act as effective barriers to latitudinal biological dispersal [26Wilson N.G. et al.Ocean barriers and glaciation: evidence for explosive radiation of mitochondrial lineages in the Antarctic sea slug Doris kerguelenensis (Mollusca, Nudibranchia).Mol. Ecol. 2009; 18: 965-984Crossref PubMed Scopus (136) Google Scholar, 27Janosik A. et al.Evolutionary history of Southern Ocean Odontaster sea star species (Odontasteridae; Asteroidea).Polar Biol. 2011; 34: 575-586Crossref Scopus (51) Google Scholar, 53González-Wevar C.A. et al.Molecular phylogeny and historical biogeography of Nacella (Patellogastropoda: Nacellidae) in the Southern Ocean.Mol. Phylogenet. Evol. 2010; 56: 115-124Crossref PubMed Scopus (69) Google Scholar, 91Wilson N. et al.Multiple lineages and absence of panmixia in the 'circumpolar' crinoid Promachocrinus kerguelensis from the Atlantic sector of Antarctica.Mar. Biol. 2007; 152: 895-904Crossref Scopus (114) Google Scholar, 92Diaz A. et al.Evolutionary pathways among shallow and deep-sea echinoids of the genus Sterechinus in the Southern Ocean.Deep Sea Res. Part II: Top. Stud. Oceanogr. 2011; 58: 205-211Crossref Scopus (66) Google Scholar], and have probably prevented many taxa from dispersing to the Antarctic and sub-Antarctic regions during warm interglacial periods, with some exceptions [93Aronson R.B. et al.Climate change and invasibility of the Antarctic benthos.Annu. Rev. Ecol. Evol. S. 2007; 38: 129-154Crossref Scopus (216) Google Scholar, 94Clarke A. et al.How isolated is Antarctica?.Trends Ecol. Evol. 2005; 20: 1-3Abstract Full Text Full Text PDF PubMed Scopus (215) Google Scholar]. Most taxa present in these southern regions are inferred to have persisted in local refugia throughout recent glaciations. By contrast, Northern Hemisphere taxa, both marine and terrestrial, highly mobile and sedentary, have experienced more dynamic histories, with major northward range shifts during interglacial periods in the absence of strong oceanographic barriers comparable to the southern ACC, APF and STC (although, in some cases, mountain ranges have limited their postglacial dispersal [1Hewitt G. The genetic legacy of the Quaternary ice ages.Nature. 2000; 405: 907-913Crossref PubMed Scopus (5120) Google Scholar]) (Figure I). As Earth has undergone cycles of global climate change, organismal distributions have shifted in response, generally moving away from the poles during glacial periods, and towards the poles during interglacials [1Hewitt G. The genetic legacy of the Quaternary ice ages.Nature. 2000; 405: 907-913Crossref PubMed Scopus (5120) Google Scholar]. Postglacial (see Glossary) recolonisation of territory made habitable by receding glaciers and warming temperatures is typically marked by a relative lack of genetic diversity in newly re-established populations. This biogeographic pattern reflects both the young age of such populations and the rapid demographic expansion of 'leading-edge' colonists, effectively blocking the establishment of later immigrants [1Hewitt G. The genetic legacy of the Quaternary ice ages.Nature. 2000; 405: 907-913Crossref PubMed Scopus (5120) Google Scholar, 2Hewitt G.M. Genetic consequences of climatic oscillations in the Quaternary.Philos. Trans. R. Soc. Lond. Ser. B. 2004; 359: 183-195Crossref PubMed Scopus (2526) Google Scholar, 3Waters J.M. Competitive exclusion: phylogeography's 'elephant in the room'?.Mol. Ecol. 2011; 20: 4388-4394Crossref PubMed Scopus (78) Google Scholar]. In the Northern Hemisphere, major postglacial ranges shifts have been inferred for a wide variety of taxa, with many species moving from mid-latitude refugia to northern habitats or to higher altitudes [2Hewitt G.M. Genetic consequences of climatic oscillations in the Quaternary.Philos. Trans. R. Soc. Lond. Ser. B. 2004; 359: 183-195Crossref PubMed Scopus (2526) Google Scholar]. Species can have highly individualistic responses to glacial–interglacial climate change, and patterns of postglacial range shifts thus vary greatly among taxa [4Stewart J.R. et al.Refugia revisited: individualistic responses of species in space and time.Proc. R. Soc. B: Biol. Sci. 2010; 277: 661-671Crossref PubMed Scopus (858) Google Scholar, 5Maggs C.A. et al.Evaluating signatures of glacial refugia for North Atlantic benthic marine taxa.Ecology. 2008; 89: S108-S122Crossref PubMed Scopus (404) Google Scholar]. Nonetheless, although some high-latitude taxa appear to have survived locally throughout the last glaciation (sometimes referred to as persistence in 'cryptic refugia') [2Hewitt G.M. Genetic consequences of climatic oscillations in the Quaternary.Philos. Trans. R. Soc. Lond. Ser. B. 2004; 359: 183-195Crossref PubMed Scopus (2526) Google Scholar, 4Stewart J.R. et al.Refugia revisited: individualistic responses of species in space and time.Proc. R. Soc. B: Biol. Sci. 2010; 277: 661-671Crossref PubMed Scopus (858) Google Scholar, 5Maggs C.A. et al.Evaluating signatures of glacial refugia for North Atlantic benthic marine taxa.Ecology. 2008; 89: S108-S122Crossref PubMed Scopus (404) Google Scholar, 6Provan J. Bennett K.D. Phylogeographic insights into cryptic glacial refugia.Trends Ecol. Evol. 2008; 23: 564-571Abstract Full Text Full Text PDF PubMed Scopus (796) Google Scholar], the overwhelming pattern in the temperate and polar Northern Hemisphere has been one of large latitudinal postglacial range shifts. In contrast to the wealth of literature addressing Northern Hemisphere climate change and biodiversity impacts, relatively few studies had, until recently, addressed the glacial–interglacial history of Southern Hemisphere ecosystems (but see [7Chown S.L. et al.Ecological biogeography of Southern Ocean islands: species–area relationships, human impacts, and conservation.Am. Nat. 1998; 152: 562-575Crossref PubMed Scopus (254) Google Scholar]). Emerging data suggest that patterns in the comparatively oceanic Southern Hemisphere (Box 1, Box 2) differ considerably from those of the Northern Hemisphere, particularly at the polar and subpolar (i.e., greater than approximately 50°S) latitudes. At a time of rapid, anthropogenically accelerated global warming [8Anderegg W.R.L. et al.Expert credibility in climate change.Proc. Natl. Acad. Sci. U.S.A. 2010; 107: 12107-12109Crossref PubMed Scopus (507) Google Scholar], understanding the factors that facilitate or inhibit biological range shifts in response to climate change is critically important. Here, we review the predominant patterns of biological response in the Southern Hemisphere high latitudes (glaciated or sea ice-affected regions) to the interglacial warming that followed the LGM, from approximately 18 000 years ago to the present day [9Denton G.H. et al.The Last Glacial Termination.Science. 2010; 328: 1652-1656Crossref PubMed Scopus (550) Google Scholar]. We consider the factors controlling high-latitude biodiversity shifts based on physical contrasts between the Northern and Southern hemispheres. We focus on biological range shifts in response to natural global warming, rather than anthropogenic invasions or human-mediated recent global warming, and primarily deal with taxa for which there is clear evidence of natural population expansion and/or range shifts since the LGM. Our focus is on the high latitudes, but we also include brief overviews of postglacial range shifts in other glaciated parts of Southern Hemisphere [i.e. New Zealand, Tasmania (Australia) and southern South America].Box 2Characteristics of Southern Hemisphere high latitudesAntarctica is a heavily glaciated continent, and parts of the surrounding ocean are covered by sea ice for much of the year, particularly in winter. Antarctica was thought to have been completely glaciated at the LGM, although new biological data indicate that some pockets of terrestrial habitat probably remained ice free [12Convey P. et al.Exploring biological constraints on the glacial history of Antarctica.Quat. Sci. Rev. 2009; 28: 3035-3048Crossref Scopus (156) Google Scholar].The sub-Antarctic islands (here considered to be those occurring approximately between the STC and the APF, but also including South Georgia and Heard Island) have diverse geological and glacial histories. At the LGM, some islands are thought to have been fully glaciated, with ice probably extending offshore (e.g., Kerguelen and Heard Islands), whereas for others there is geological evidence that some terrestrial areas remained ice free (e.g., on Crozet, Falkland and Macquarie islands) [96Hall K. Quaternary glaciation of the sub-Antarctic Islands.in: Ehlers J. Gibbard P.L. Quaternary Glaciations – Extent and Chronology, Part III. Elsevier, 2004: 339-345Google Scholar]. However, in many cases, the extent of glaciation on sub-Antarctic islands remains poorly known (see [38Van der Putten N. et al.Subantarctic flowering plants: pre-glacial survivors or post-glacial immigrants?.J. Biogeogr. 2010; 37: 582-592Crossref Scopus (65) Google Scholar]), and the possibility of LGM terrestrial glacial refugia cannot be dismissed for any. Antarctic winter sea ice extended considerably further north at the LGM than it does today and, although the precise extent of the ice is not known [50Gersonde R. et al.Sea-surface temperature and sea ice distribution of the Southern Ocean at the EPILOG Last Glacial Maximum – a circum-Antarctic view based on siliceous microfossil records.Quat. Sci. Rev. 2005; 24: 869-896Crossref Scopus (408) Google Scholar], there is some biological indication that it at least occasionally extended north to sub-Antarctic islands, such as Macquarie, Marion and Crozet Islands [46Fraser C.I. et al.Kelp genes reveal effects of subantarctic sea ice during the Last Glacial Maximum.Proc. Natl. Acad. Sci. U.S.A. 2009; 106: 3249-3253Crossref PubMed Scopus (218) Google Scholar].The ocean surrounding Antarctica (the Southern Ocean) connects the Atlantic, Pacific and Indian Oceans and is home to the strongest current in the world, the ACC, driven largely by intense westerly winds. Cold Antarctic waters meet warmer sub-Antarctic waters at the APF (also known as the Antarctic Convergence), and sub-Antarctic waters extend north to the STC (Figure I). Antarctica is a heavily glaciated continent, and parts of the surrounding ocean are covered by sea ice for much of the year, particularly in winter. Antarctica was thought to have been completely glaciated at the LGM, although new biological data indicate that some pockets of terrestrial habitat probably remained ice free [12Convey P. et al.Exploring biological constraints on the glacial history of Antarctica.Quat. Sci. Rev. 2009; 28: 3035-3048Crossref Scopus (156) Google Scholar]. The sub-Antarctic islands (here considered to be those occurring approximately between the STC and the APF, but also including South Georgia and Heard Island) have diverse geological and glacial histories. At the LGM, some islands are thought to have been fully glaciated, with ice probably extending offshore (e.g., Kerguelen and Heard Islands), whereas for others there is geological evidence that some terrestrial areas remained ice free (e.g., on Crozet, Falkland and Macquarie islands) [96Hall K. Quaternary glaciation of the sub-Antarctic Islands.in: Ehlers J. Gibbard P.L. Quaternary Glaciations – Extent and Chronology, Part III. Elsevier, 2004: 339-345Google Scholar]. However, in many cases, the extent of glaciation on sub-Antarctic islands remains poorly known (see [38Van der Putten N. et al.Subantarctic flowering plants: pre-glacial survivors or post-glacial immigrants?.J. Biogeogr. 2010; 37: 582-592Crossref Scopus (65) Google Scholar]), and the possibility of LGM terrestrial glacial refugia cannot be dismissed for any. Antarctic winter sea ice extended considerably further north at the LGM than it does today and, although the precise extent of the ice is not known [50Gersonde R. et al.Sea-surface temperature and sea ice distribution of the Southern Ocean at the EPILOG Last Glacial Maximum – a circum-Antarctic view based on siliceous microfossil records.Quat. Sci. Rev. 2005; 24: 869-896Crossref Scopus (408) Google Scholar], there is some biological indication that it at least occasionally extended north to sub-Antarctic islands, such as Macquarie, Marion and Crozet Islands [46Fraser C.I. et al.Kelp genes reveal effects of subantarctic sea ice during the Last Glacial Maximum.Proc. Natl. Acad. Sci. U.S.A. 2009; 106: 3249-3253Crossref PubMed Scopus (218) Google Scholar]. The ocean surrounding Antarctica (the Southern Ocean) connects the Atlantic, Pacific and Indian Oceans and is home to the strongest current in the world, the ACC, driven largely by intense westerly winds. Cold Antarctic waters meet warmer sub-Antarctic waters at the APF (also known as the Antarctic Convergence), and sub-Antarctic waters extend north to the STC (Figure I). Only approximately 0.3% of Antarctica is currently ice free [10Convey P. Stevens M.I. Antarctic biodiversity.Science. 2007; 317: 1877-1878Crossref PubMed Scopus (149) Google Scholar], and it has long been thought that little or no ice-free habitat could have existed at the LGM [11Convey P. et al.Antarctic terrestrial life – challenging the history of the frozen continent?.Biol. Rev. 2008; 83: 103-117Crossref PubMed Scopus (256) Google Scholar]. However, numerous recent studies provide evidence of deeply divergent lineages unique to Antarctica, indicating glacial survival in fragmented habitats followed by postglacial expansion, and pointing to long-term persistence of terrestrial taxa, such as arthropods, on the Antarctic continent [11Convey P. et al.Antarctic terrestrial life – challenging the history of the frozen continent?.Biol. Rev. 2008; 83: 103-117Crossref PubMed Scopus (256) Google Scholar, 12Convey P. et al.Exploring biological constraints on the glacial history of Antarctica.Quat. Sci. Rev. 2009; 28: 3035-3048Crossref Scopus (156) Google Scholar, 13McGaughran A. et al.Extreme glacial legacies: a synthesis of the Antarctic springtail phylogeographic record.Insects. 2011; 2: 62-82Crossref Scopus (30) Google Scholar, 14McGaughran A. et al.Biogeography of circum-Antarctic springtails.Mol. Phylogenet. Evol. 2010; 57: 48-58Crossref PubMed Scopus (30) Google Scholar, 15De Wever A. et al.Hidden levels of phylodiversity in Antarctic green algae: further evidence for the existence of glacial refugia.Proc. R. Soc. B: Biol. Sci. 2009; 276: 3591-3599Crossref PubMed Scopus (126) Google Scholar, 16Allegrucci G. et al.A molecular phylogeny of Antarctic chironomidae and its implications for biogeographical history.Polar Biol. 2006; 29: 320-326Crossref Scopus (94) Google Scholar]. The only evidence of postglacial recolonisation of the Antarctic from lower latitudes comes from highly dispersive marine mammals and seabirds (Box 3). Some endemic freshwater copepods and cladocerans appear to have survived the last Ice Age in Antarctica [12Convey P. et al.Exploring biological constraints on the glacial history of Antarctica.Quat. Sci. Rev. 2009; 28: 3035-3048Crossref Scopus (156) Google Scholar], and ancient lineages of Antarctic mites, estimated to have diverged from their non-Antarctic sister groups 6–10 million years ago (Mya), have presumably also persisted on the continent throughout numerous glacial periods [17Mortimer E. et al.Mite dispersal among the Southern Ocean Islands and Antarctica before the Last Glacial Maximum.Proc. R. Soc. B: Biol. Sci. 2011; 278: 1247-1255Crossref PubMed Scopus (55) Google Scholar]. The biogeographic history of the two vascular plant taxa native to Antarctica is not well understood, and whether they are ancient Gondwanan relicts or postglacial colonists has yet to be resolved [18Mosyakin S. et al.Origins of native vascular plants of Antarctica: comments from a historical phytogeography viewpoint.Cytol. Genet. 2007; 41: 308-316Crossref Google Scholar]. For the non-vascular flora, many lichens (33–50%) appear to be endemic, and so are likely to have survived recent glacial periods locally in Antarctica. By contrast, many mosses (6–7% endemic) are proposed to be recent, potentially postglacial, colonists, possibly arriving via wind-driven propagule dispersal from neighbouring landmasses [19Peat H.J. et al.Diversity and biogeography of the Antarctic flora.J. Biogeogr. 2007; 34: 132-146Crossref Scopus (149) Google Scholar]. However, molecular work indicates that Antarctic moss endemism might currently be underestimated, and also provides evidence for Pleistocene persistence for some lineages in Victoria Land refugia (Figure 1) [20Hills S.F.K. et al.Molecular support for Pleistocene persistence of the continental Antarctic moss Bryum argenteum.Antarct. Sci. 2010; 22: 721-726Crossref Scopus (21) Google Scholar].Box 3Postglacial recolonisation of Antarctica by marine mammals and seabirdsOnly for marine mammals and seabirds, capable of travelling long distances in short periods of time, have any large latitudinal range shifts been inferred in the Antarctic since the LGM. Species that require icy environments (ice obligates) should theoretically not have been particularly adversely impacted by Pleistocene glaciations, whereas those that form colonies on ice-free land (e.g., gentoo penguins, Adélie penguins, fur seals, elephant seals and sea lions) would have had to retreat to lower latitudes during glacial maxima, at least for breeding purposes. In the Northern Hemisphere, several Arctic marine mammals, although cold-adapted and highly dispersive, show signatures of classic south-to-north postglacial range shifts, with population segregation and bottlenecks inferred at the LGM [98O'Corry-Crowe G. Climate change and the molecular ecology of Arctic marine mammals.Ecol. Appl. 2008; 18: S56-S76Crossref PubMed Scopus (41) Google Scholar]. A molecular study of extant and extinct sub-Antarctic and Antarctic elephant seal (Mirounga leonina) populations, a species that requires ice-free land to breed, indicates that an Antarctic continent (Victoria Land) population colonised the area when it was freed from ice 7500–8000 years ago, but was driven out by ice growth approximately 1000 years ago to again take refuge at lower-latitude Macquarie Island, where the species is still found [84de Bruyn M. et al.Rapid response of a marine mammal species to Holocene climate and habitat change.PLoS Genet. 2009; 5: e1000554Crossref PubMed Scopus (77) Google Scholar] (Figure 1, main text). Similarly, with glacial shortage of coastal polynyas for feeding and ice-free land for nesting, it has been proposed that all Antarctic penguin species except the emperor (Aptenodytes forsteri) might have retreated to lower latitude (sub-Antarctic) refugia to breed during glacial maxima [25Thatje S. et al.Life hung by a thread: endurance of Antarctic fauna in glacial periods.Ecology. 2008; 89: 682-692Crossref PubMed Scopus (122) Google Scholar]. Genetic evidence indicates that modern Adélie penguins derive from two lineages, presumably from two refugial populations of uncertain location (but potentially within the Antarctic region) that expanded after the last ice age [99Ritchie P.A. et al.Ancient DNA enables timing of the Pleistocene origin and Holocene expansion of two Adélie penguin lineages in Antarctica.Mol. Biol. Evol. 2004; 21: 240-248Crossref PubMed Scopus (83) Google Scholar]. In contrast to penguins, some flighted seabirds, such as petrels, are able to nest on nunataks and fly to open-ocean polynyas to feed, and thus might well have persisted in situ throughout recent glacial periods [25Thatje S. et al.Life hung by a thread: endurance of Antarctic fauna in glacial periods.Ecology. 2008; 89: 682-692Crossref PubMed Scopus (122) Google Scholar]. Only for marine mammals and seabirds, capable of travelling long distances in short periods of time, have any large latitudinal range shifts been inferred in the Antarctic since the LGM. Species that require icy environments (ice obligates) should theoretically not have been particularly adversely impacted by Pleistocene glaciations, whereas those that form colonies on ice-free land (e.g., gentoo penguins, Adélie penguins, fur seals, elephant seals and sea lions) would have had to retreat to lower latitudes during glacial maxima, at least for breeding purposes. In the Northern Hemisphere, several Arctic marine mammals, although cold-adapted and highly dispersive, show signatures of classic south-to-north postglacial range shifts, with population segregation and bottlenecks inferred at the LGM [98O'Corry-Crowe G. Climate change and the molecular ecology of Arctic marine mammals.Ecol. Appl. 2008; 18: S56-S76Crossref PubMed Scopus (41) Google Scholar]. A molecular study of extant and extinct sub-Antarctic and Antarctic elephant seal (Mirounga leonina) populations, a species that requires ice-free land to breed, indicates that an Antarctic continent (Victoria Land) population colonised the area when it was freed from ice 7500–8000 years ago, but was driven out by ice growth approximately 1000 years ago to again take refuge at lower-latitude Macquarie Island, where the species is still found [84de Bruyn M. et al.Rapid response of a marine mammal species to Holocene climate and habitat change.PLoS Genet. 2009; 5: e1000554Crossref PubMed Scopus (77) Google Scholar] (Figure 1, main text). Similarly, with glacial shortage of coastal polynyas for feeding and ice-free land for nesting, it has been proposed that all Antarctic penguin species except the emperor (Aptenodytes forsteri) might have retreated to lower latitude (sub-Antarctic) refugia to breed during glacial maxima [25Thatje S. et al.Life hung by a thread: endurance of Antarctic fauna in glacial periods.Ecology. 2008; 89: 682-692Crossref PubMed Scopus (122) Google Scholar]. Genetic evidence indicates that modern Adélie penguins derive from two lineages, presumably from two refugial populations of uncertain location (but potentially within the Antarctic region) that expanded after the last ice age [99Ritchie P.A. et al.Ancient DNA enables timing of the Pleistocene origin and Holocene expansion of two Adélie penguin lineages in Antarctica.Mol. Biol. Evol. 2004; 21: 240-248Crossref PubMed Scopus (83) Google Scholar]. In contrast to penguins, some flighted seabirds, such as petrels, are able to nest on nunataks and fly to open-ocean polynyas to feed, and thus might well have persisted in situ throughout recent glacial periods [25Thatje S. et al.Life hung by a thread: endurance of Antarctic fauna in glacial periods.Ecology. 2008; 89: 682-692Crossref PubMed Scopus (122) Google Scholar]. The existence of ice-free pockets of terrestrial habitat throughout recent ice ages is supported by numerous molecular studies of Antarctic taxa, and possible locations of Antarctic ice-free terrestrial glacial refugia have been inferred from genetic evidence of ancient lineages [12Convey P. et al.Exploring biological constraints on the glacial history of Antarctica.Quat. Sci. Rev. 2009; 28: 3035-3048Crossref Scopus (156) Google Scholar] (Figure 1), yet geological evidence for such refugia remains scant [11Convey P. et al.Antarctic terrestrial life – challenging the history of the frozen continent?.Biol. Rev. 2008; 83: 103-117Crossref PubMed Scopus (256) Google Scholar]. Collapse of the West Antarctic Ice Sheet during some Pleistocene interglacials [21Pollard D. DeConto R.M. Modelling West Antarctic Ice Sheet growth and collapse through the past five million years.Nature. 2009; 458: 329-332Crossref PubMed Scopus (680) Google Scholar] might have created a more maritime environment close to the Transantarctic Mountains, promoting dispersal of terrestrial taxa during interglacials and thereby increasing their chances of glacial survival. Small ice-free areas, such as nunataks (e.g., in alpine regions such as the Transantarctic Mountains), probably existed during recent glacial periods, potentially providing refugia throughout the LGM for alpine taxa (e.g., the endemic montane mite family Maudheimiidae) [11Convey P. et al.Antarctic terrestrial life – challenging the history of the frozen continent?.Biol. Rev. 2008; 83: 103-117Crossref PubMed Scopus (256) Google Scholar]. However, nunatak fauna are primarily continental and alpine specialised; therefore, the persistence of lower altitude fauna throughout the LGM cannot easily be explained by nunataks [11Convey P. et al.Antarctic terrestrial life – challenging the history of the frozen continent?.Biol. Rev. 2008; 83: 103-117Crossref PubMed Scopus (256) Google Scholar]. Pockets of relatively warm, ice-free land within mouths of geothermal glacial caves, or areas around volcanoes made ice free by volcanic steam, could explain the glacial persistence of some Antarctic terrestrial taxa. There is presently an extensive geothermal cave system
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