The latitudinal biodiversity gradient through deep time
Authors: Philip D. Mannion, Paul Upchurch, Roger B.J. Benson, Anjali Goswami
Journal: Trends in Ecology & Evolution (2013)

•The latitudinal biodiversity gradient has not been a persistent feature through time.•The modern pattern might only have originated 30 million years ago.•A temperate diversity peak is recorded during warmer intervals.•A tropical diversity peak might characterise icehouse worlds. Today, biodiversity decreases from equatorial to polar regions. This is a fundamental pattern governing the distribution of extant organisms, the understanding of which is critical to predicting climatically driven biodiversity loss. However, its causes remain unresolved. The fossil record offers a unique perspective on the evolution of this latitudinal biodiversity gradient (LBG), providing a dynamic system in which to explore spatiotemporal diversity fluctuations. Deep-time studies indicate that a tropical peak and poleward decline in species diversity has not been a persistent pattern throughout the Phanerozoic, but is restricted to intervals of the Palaeozoic and the past 30 million years. A tropical peak might characterise cold icehouse climatic regimes, whereas warmer greenhouse regimes display temperate diversity peaks or flattened gradients. Today, biodiversity decreases from equatorial to polar regions. This is a fundamental pattern governing the distribution of extant organisms, the understanding of which is critical to predicting climatically driven biodiversity loss. However, its causes remain unresolved. The fossil record offers a unique perspective on the evolution of this latitudinal biodiversity gradient (LBG), providing a dynamic system in which to explore spatiotemporal diversity fluctuations. Deep-time studies indicate that a tropical peak and poleward decline in species diversity has not been a persistent pattern throughout the Phanerozoic, but is restricted to intervals of the Palaeozoic and the past 30 million years. A tropical peak might characterise cold icehouse climatic regimes, whereas warmer greenhouse regimes display temperate diversity peaks or flattened gradients. The present-day decrease in biological diversity from equatorial to polar regions (Figure 1) is a pervasive pattern governing the distribution of life on Earth [1Willig M.R. et al.Latitudinal gradients of biodiversity: pattern, process, scale, and synthesis.Annu. Rev. Ecol. Evol. Syst. 2003; 34: 273-309Crossref Scopus (1482) Google Scholar, 2Hillebrand H. On the generality of the latitudinal diversity gradient.Am. Nat. 2004; 163: 192-211Crossref PubMed Scopus (1330) Google Scholar]. Attempts to explain this LBG have tended to ignore a deep-time perspective. Here, we redress this balance by bringing together data on the past distribution of biodiversity and examine what this reveals about the underlying causes of the LBG. Before moving to a more palaeontological viewpoint, it is useful to summarise briefly what is known of the present-day LBG. This gradient describes most fauna and flora, in both terrestrial and marine realms, in both hemispheres, and across a range of spatial scales [1Willig M.R. et al.Latitudinal gradients of biodiversity: pattern, process, scale, and synthesis.Annu. Rev. Ecol. Evol. Syst. 2003; 34: 273-309Crossref Scopus (1482) Google Scholar, 2Hillebrand H. On the generality of the latitudinal diversity gradient.Am. Nat. 2004; 163: 192-211Crossref PubMed Scopus (1330) Google Scholar, 3Field R. et al.Spatial species-richness gradients across scales: a meta-analysis.J. Biogeogr. 2009; 36: 132-147Crossref Scopus (534) Google Scholar]. Some clades provide exceptions to this pattern [4Krug A.Z. et al.Contrarian clade confirms the ubiquity of spatial origination patterns in the production of latitudinal diversity gradients.Proc. Natl. Acad. Sci. U.S.A. 2007; 104: 18129-18134Crossref PubMed Scopus (33) Google Scholar, 5Kiel S. Nielson S.N. Quaternary origin of the inverse latitudinal diversity gradient among southern Chilean mollusks.Geology. 2012; 38: 955-958Crossref Scopus (42) Google Scholar], including temperate peaks in most salamander and frog families [6Wiens J.J. Global patterns of diversification and species richness in amphibians.Am. Nat. 2007; 170: 86-106Crossref Scopus (214) Google Scholar], as well as some aquatic birds and mammals [7Chown S.L. et al.Global patterns in species richness of pelagic seabirds: the Procellariiformes.Ecography. 1998; 21: 342-350Crossref Scopus (36) Google Scholar, 8Proches S. Back to the sea: secondary marine organisms from a biogeographical perspective.Biol. J. Linn. Soc. 2001; 74: 197-203Google Scholar, 9Tittensor D.P. et al.Global patterns and predictors of marine biodiversity across taxa.Nature. 2010; 466: 1098-1101Crossref PubMed Scopus (988) Google Scholar], but contrarian groups are otherwise predominantly limited to aquatic floras and parasitic species [1Willig M.R. et al.Latitudinal gradients of biodiversity: pattern, process, scale, and synthesis.Annu. Rev. Ecol. Evol. Syst. 2003; 34: 273-309Crossref Scopus (1482) Google Scholar]. Examples of hemispherical asymmetry in biodiversity also exist, such as low ant biodiversity in the Northern Hemisphere, which tend to reflect either recent climatic differences, or evolutionary events, such as localised extinctions [10Chown S.L. et al.Hemispherical asymmetries in biodiversity: a serious matter for ecology.PLoS Biol. 2004; 2: e406Crossref PubMed Scopus (125) Google Scholar, 11Dunn R.R. et al.Climatic drivers of hemispheric asymmetry in global patterns of ant species richness.Ecol. Lett. 2009; 12: 324-333Crossref PubMed Scopus (220) Google Scholar, 12Archibald S.B. et al.Seasonality, the latitudinal gradient of diversity, and Eocene insects.Paleobiology. 2010; 36: 374-398Crossref Scopus (118) Google Scholar, 13Krug A.Z. et al.Differential extinction and the contrasting structure of polar marine faunas.PLoS ONE. 2010; 5: e15362Crossref PubMed Scopus (28) Google Scholar]. Most often in these instances, there is heightened overall diversity in one hemisphere, but it is rare that a tropical peak in species diversity exists in one hemisphere but not the other [10Chown S.L. et al.Hemispherical asymmetries in biodiversity: a serious matter for ecology.PLoS Biol. 2004; 2: e406Crossref PubMed Scopus (125) Google Scholar, 11Dunn R.R. et al.Climatic drivers of hemispheric asymmetry in global patterns of ant species richness.Ecol. Lett. 2009; 12: 324-333Crossref PubMed Scopus (220) Google Scholar, 12Archibald S.B. et al.Seasonality, the latitudinal gradient of diversity, and Eocene insects.Paleobiology. 2010; 36: 374-398Crossref Scopus (118) Google Scholar, 13Krug A.Z. et al.Differential extinction and the contrasting structure of polar marine faunas.PLoS ONE. 2010; 5: e15362Crossref PubMed Scopus (28) Google Scholar]. However, these are exceptions to the rule, and the LBG is regarded as the dominant first-order macroecological pattern on Earth today [14Krug A.Z. et al.Generation of Earth's first-order biodiversity pattern.Astrobiology. 2009; 9: 113-124Crossref PubMed Scopus (73) Google Scholar]. Understanding the causes and evolution of the LBG is critical to explaining present-day geographical variation in biodiversity and modelling biotic responses to climate change (e.g., [15Orme C.D.L. et al.Global hotspots of species richness are not congruent with endemism or threat.Nature. 2005; 436: 1016-1019Crossref PubMed Scopus (905) Google Scholar, 16Colwell R.K. et al.Global warming, elevational range shifts, and lowland biotic attrition in the wet tropics.Science. 2008; 322: 258-261Crossref PubMed Scopus (922) Google Scholar, 17Deutsch C.A. et al.Impacts of climate warming on terrestrial ectotherms across latitude.Proc. Natl. Acad. Sci. U.S.A. 2008; 105: 6668-6672Crossref PubMed Scopus (2492) Google Scholar, 18Jenkins C.N. et al.Global patterns of terrestrial vertebrate diversity and conservation.Proc. Natl. Acad. Sci. U.S.A. 2013; 110: 11457-11462Crossref PubMed Scopus (67) Google Scholar]). Net diversification rates are higher in the tropics than elsewhere [19Wiens J.J. Donoghue M.J. Historical biogeography, ecology and species richness.Trends Ecol. Evol. 2004; 19: 639-644Abstract Full Text Full Text PDF PubMed Scopus (1309) Google Scholar, 20Cardillo M. et al.Testing for latitudinal bias in diversification rates: an example using New World birds.Ecology. 2005; 86: 2278-2287Crossref Scopus (146) Google Scholar, 21Jablonski D. et al.Out of the tropics: evolutionary dynamics of the latitudinal diversity gradient.Science. 2006; 314: 102-106Crossref PubMed Scopus (626) Google Scholar, 22Mittelbach G.G. et al.Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography.Ecol. Lett. 2007; 10: 315-331Crossref PubMed Scopus (1202) Google Scholar, 23Weir J.T. Schluter D. The latitudinal gradient in recent speciation and extinction rates of birds and mammals.Science. 2007; 315: 1574-1576Crossref PubMed Scopus (414) Google Scholar]. However, it is unclear whether this reflects relatively higher origination rates, lower extinction rates, or both (Box 1), and dispersal likely further complicates this picture [14Krug A.Z. et al.Generation of Earth's first-order biodiversity pattern.Astrobiology. 2009; 9: 113-124Crossref PubMed Scopus (73) Google Scholar, 21Jablonski D. et al.Out of the tropics: evolutionary dynamics of the latitudinal diversity gradient.Science. 2006; 314: 102-106Crossref PubMed Scopus (626) Google Scholar, 22Mittelbach G.G. et al.Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography.Ecol. Lett. 2007; 10: 315-331Crossref PubMed Scopus (1202) Google Scholar, 24Martin P.R. et al.Revisiting Jablonski (1993): cladogenesis and range expansion explain latitudinal variation in taxonomic richness.J. Evol. Biol. 2007; 20: 930-936Crossref PubMed Scopus (27) Google Scholar, 25Roy K. Goldberg E.E. Origination, extinction and dispersal: integrative models for understanding present-day diversity gradients.Am. Nat. 2007; 170: 71-85Crossref Scopus (93) Google Scholar, 26Jocque M. et al.Climatic control of dispersal–ecological specialization trade-offs: a metacommunity process at the heart of the latitudinal diversity gradient?.Global Ecol. Biogeogr. 2010; 19: 244-252Crossref Scopus (113) Google Scholar, 27Soria-Carrasco V. Castresana J. Diversification rates and the latitudinal gradient of diversity in mammals.Proc. R. Soc. Lond. B: Biol. Sci. 2012; 279: 4148-4155Crossref Scopus (48) Google Scholar, 28Jablonski D. et al.Out of the tropics, but how? Fossils, bridge species, and thermal ranges in the dynamics of the marine latitudinal diversity gradient.Proc. Natl. Acad. Sci. U.S.A. 2013; 110: 10487-10494Crossref PubMed Scopus (166) Google Scholar]. Despite a long history of study, the causes of the LBG remain unresolved [1Willig M.R. et al.Latitudinal gradients of biodiversity: pattern, process, scale, and synthesis.Annu. Rev. Ecol. Evol. Syst. 2003; 34: 273-309Crossref Scopus (1482) Google Scholar, 2Hillebrand H. On the generality of the latitudinal diversity gradient.Am. Nat. 2004; 163: 192-211Crossref PubMed Scopus (1330) Google Scholar]. Most hypotheses can be rejected on the grounds of being circular, interlinked, or too specific to explain the ubiquity of the gradient, leaving three broad (although not necessarily mutually exclusive) themes for explaining higher tropical rates of net diversification and the modern-day LBG: (i) climatic (see below); (ii) geographical, pertaining to the greater areal extent of the tropics being able to support more species compared with other regions [29Rosenzweig M.L. Species Diversity in Space and Time. Cambridge University Press, 1995Crossref Google Scholar]; and (iii) historical, whereby the tropics have been less perturbed in the past by climatic events (e.g., the Pleistocene glaciations) and, thus, have accumulated species over a longer, uninterrupted time period compared with the extratropical regions [1Willig M.R. et al.Latitudinal gradients of biodiversity: pattern, process, scale, and synthesis.Annu. Rev. Ecol. Evol. Syst. 2003; 34: 273-309Crossref Scopus (1482) Google Scholar, 3Field R. et al.Spatial species-richness gradients across scales: a meta-analysis.J. Biogeogr. 2009; 36: 132-147Crossref Scopus (534) Google Scholar, 19Wiens J.J. Donoghue M.J. Historical biogeography, ecology and species richness.Trends Ecol. Evol. 2004; 19: 639-644Abstract Full Text Full Text PDF PubMed Scopus (1309) Google Scholar, 22Mittelbach G.G. et al.Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography.Ecol. Lett. 2007; 10: 315-331Crossref PubMed Scopus (1202) Google Scholar].Box 1Tropics as cradles, museums, or both?Attempts to explain the 'modern-type' LBG as a product of latitudinal variation in evolutionary dynamics have focussed on differences in net diversification rates [22Mittelbach G.G. et al.Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography.Ecol. Lett. 2007; 10: 315-331Crossref PubMed Scopus (1202) Google Scholar], with the species-rich tropics often regarded as either a 'cradle' (Figure IA) that generates new species (i.e., origination rates are higher in tropical areas and extinction rates do not vary latitudinally), or a 'museum' (Figure IB) that preserves existing species over time (i.e., origination rates are constant, but extinction rates are lower in the tropics) [14Krug A.Z. et al.Generation of Earth's first-order biodiversity pattern.Astrobiology. 2009; 9: 113-124Crossref PubMed Scopus (73) Google Scholar, 22Mittelbach G.G. et al.Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography.Ecol. Lett. 2007; 10: 315-331Crossref PubMed Scopus (1202) Google Scholar, 79Chown S.L. Gaston K.J. Areas, cradles and museums: the latitudinal gradient in species richness.Trends Ecol. Evol. 2000; 15: 311-315Abstract Full Text Full Text PDF PubMed Scopus (218) Google Scholar, 80Rull V. Neotropical diversity: timing and potential drivers.Trends Ecol. Evol. 2011; 26: 508-513Abstract Full Text Full Text PDF PubMed Scopus (293) Google Scholar]. These two putative causal factors are not mutually exclusive. Indeed, many studies have found evidence for higher rates of speciation in the tropics [4Krug A.Z. et al.Contrarian clade confirms the ubiquity of spatial origination patterns in the production of latitudinal diversity gradients.Proc. Natl. Acad. Sci. U.S.A. 2007; 104: 18129-18134Crossref PubMed Scopus (33) Google Scholar, 14Krug A.Z. et al.Generation of Earth's first-order biodiversity pattern.Astrobiology. 2009; 9: 113-124Crossref PubMed Scopus (73) Google Scholar, 21Jablonski D. et al.Out of the tropics: evolutionary dynamics of the latitudinal diversity gradient.Science. 2006; 314: 102-106Crossref PubMed Scopus (626) Google Scholar, 44Jablonski D. Extinction and the spatial dynamics of biodiversity.Proc. Natl. Acad. Sci. U.S.A. 2008; 105: 11528-11535Crossref PubMed Scopus (137) Google Scholar, 46Krug A.Z. Patzkowsky M.E. Geographic variation in turnover and recovery from the Late Ordovician mass extinction.Paleobiology. 2007; 33: 435-454Crossref Scopus (43) Google Scholar, 81Allen A.P. Gillooly J.F. Assessing latitudinal gradients in speciation rates and biodiversity at the global scale.Ecol. Lett. 2006; 9: 947-954Crossref PubMed Scopus (168) Google Scholar, 82Allen A.P. et al.Kinetic effects of temperature on rates of genetic divergence and speciation.Proc. Natl. Acad. Sci. U.S.A. 2006; 103: 9130-9135Crossref PubMed Scopus (323) Google Scholar, 83McKenna D.D. Farrell B.D. Tropical forests are both evolutionary cradles and museums of leaf beetle diversity.Proc. Natl. Acad. Sci. U.S.A. 2006; 103: 10947-10951Crossref PubMed Scopus (176) Google Scholar, 84Eo S.H. et al.Population divergence in plant species reflects latitudinal diversity gradients.Biol. Lett. 2008; 4: 382-384Crossref PubMed Scopus (37) Google Scholar, 85Kiessling W. et al.Reefs as cradles of evolution and sources of biodiversity in the Phanerozoic.Science. 2010; 327: 196-198Crossref PubMed Scopus (127) Google Scholar], and a few analyses have demonstrated lower tropical rates of extinction [21Jablonski D. et al.Out of the tropics: evolutionary dynamics of the latitudinal diversity gradient.Science. 2006; 314: 102-106Crossref PubMed Scopus (626) Google Scholar, 23Weir J.T. Schluter D. The latitudinal gradient in recent speciation and extinction rates of birds and mammals.Science. 2007; 315: 1574-1576Crossref PubMed Scopus (414) Google Scholar, 83McKenna D.D. Farrell B.D. Tropical forests are both evolutionary cradles and museums of leaf beetle diversity.Proc. Natl. Acad. Sci. U.S.A. 2006; 103: 10947-10951Crossref PubMed Scopus (176) Google Scholar]. It seems that the tropics might act as both a cradle and museum for biodiversity [21Jablonski D. et al.Out of the tropics: evolutionary dynamics of the latitudinal diversity gradient.Science. 2006; 314: 102-106Crossref PubMed Scopus (626) Google Scholar, 22Mittelbach G.G. et al.Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography.Ecol. Lett. 2007; 10: 315-331Crossref PubMed Scopus (1202) Google Scholar, 83McKenna D.D. Farrell B.D. Tropical forests are both evolutionary cradles and museums of leaf beetle diversity.Proc. Natl. Acad. Sci. U.S.A. 2006; 103: 10947-10951Crossref PubMed Scopus (176) Google Scholar]: Jablonski et al. [21Jablonski D. et al.Out of the tropics: evolutionary dynamics of the latitudinal diversity gradient.Science. 2006; 314: 102-106Crossref PubMed Scopus (626) Google Scholar, 28Jablonski D. et al.Out of the tropics, but how? Fossils, bridge species, and thermal ranges in the dynamics of the marine latitudinal diversity gradient.Proc. Natl. Acad. Sci. U.S.A. 2013; 110: 10487-10494Crossref PubMed Scopus (166) Google Scholar] proposed an 'out of the tropics' model (Figure IC), in which origination rates are higher in the tropics and taxa disperse polewards without losing their tropical presence [14Krug A.Z. et al.Generation of Earth's first-order biodiversity pattern.Astrobiology. 2009; 9: 113-124Crossref PubMed Scopus (73) Google Scholar, 86Valentine J.W. et al.Incumbency, diversity and latitudinal gradients.Paleobiology. 2008; 34: 169-178Crossref Scopus (76) Google Scholar]. However, aspects of all of these models have been questioned: (i) Weir and Schluter [23Weir J.T. Schluter D. The latitudinal gradient in recent speciation and extinction rates of birds and mammals.Science. 2007; 315: 1574-1576Crossref PubMed Scopus (414) Google Scholar] recovered elevated rates of origination at higher latitudes in recent birds and mammals; (ii) higher extinction rates in the tropics were reported for marine invertebrates [24Martin P.R. et al.Revisiting Jablonski (1993): cladogenesis and range expansion explain latitudinal variation in taxonomic richness.J. Evol. Biol. 2007; 20: 930-936Crossref PubMed Scopus (27) Google Scholar] and through simulations [87Arita H.T. Vázquez-Domínguez E. The tropics: cradle, museum or casino? A dynamic null model for latitudinal gradients of species diversity.Ecol. Lett. 2008; 11: 653-663Crossref PubMed Scopus (46) Google Scholar]; (iii) polar extinction rates in bivalves have been found to be lower than temperate rates [13Krug A.Z. et al.Differential extinction and the contrasting structure of polar marine faunas.PLoS ONE. 2010; 5: e15362Crossref PubMed Scopus (28) Google Scholar]; and (iv) other authors have found no evidence for a correlation between diversification rates and latitude at all for a range of groups (e.g., birds, frogs, Foraminifera, and mammals) and through simulation studies [22Mittelbach G.G. et al.Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography.Ecol. Lett. 2007; 10: 315-331Crossref PubMed Scopus (1202) Google Scholar, 27Soria-Carrasco V. Castresana J. Diversification rates and the latitudinal gradient of diversity in mammals.Proc. R. Soc. Lond. B: Biol. Sci. 2012; 279: 4148-4155Crossref Scopus (48) Google Scholar, 88Wiens J.J. et al.Evolutionary and ecological causes of the latitudinal diversity gradient in hylid frogs: tree frogs unearth the roots of high tropical diversity.Am. Nat. 2006; 168: 579-596Crossref PubMed Scopus (351) Google Scholar, 89Escarguel G. et al.Evolutionary rates do not drive latitudinal diversity gradients.J. Zool. Syst. Evol. Res. 2008; 46: 82-86Crossref Scopus (19) Google Scholar, 90Buzas M.A. Culver S.J. Geographic origin of species: the temperate-tropical interchange.Geology. 2009; 37: 879-881Crossref Scopus (8) Google Scholar, 91Jetz W. et al.The global diversity of birds in space and time.Nature. 2012; 491: 444-448Crossref PubMed Scopus (2169) Google Scholar].Consequently, support for the cradle and museum hypotheses, or some combination of them, is controversial. It is possible that the timing of origination and extinction might have some role, including whether such events occurred during icehouse or greenhouse worlds, or at times of steep or shallow climatic gradients. Clade-specific events might also make a difference; for example, post-Eocene ants have suffered greater levels of extinction in the Northern than in the Southern Hemisphere [11Dunn R.R. et al.Climatic drivers of hemispheric asymmetry in global patterns of ant species richness.Ecol. Lett. 2009; 12: 324-333Crossref PubMed Scopus (220) Google Scholar]. Currently, most studies that have examined latitudinal patterns in diversification rates have been restricted to the past 30 myr: analyses extending further back in time might help tease apart the relative influence of these different factors. Attempts to explain the 'modern-type' LBG as a product of latitudinal variation in evolutionary dynamics have focussed on differences in net diversification rates [22Mittelbach G.G. et al.Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography.Ecol. Lett. 2007; 10: 315-331Crossref PubMed Scopus (1202) Google Scholar], with the species-rich tropics often regarded as either a 'cradle' (Figure IA) that generates new species (i.e., origination rates are higher in tropical areas and extinction rates do not vary latitudinally), or a 'museum' (Figure IB) that preserves existing species over time (i.e., origination rates are constant, but extinction rates are lower in the tropics) [14Krug A.Z. et al.Generation of Earth's first-order biodiversity pattern.Astrobiology. 2009; 9: 113-124Crossref PubMed Scopus (73) Google Scholar, 22Mittelbach G.G. et al.Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography.Ecol. Lett. 2007; 10: 315-331Crossref PubMed Scopus (1202) Google Scholar, 79Chown S.L. Gaston K.J. Areas, cradles and museums: the latitudinal gradient in species richness.Trends Ecol. Evol. 2000; 15: 311-315Abstract Full Text Full Text PDF PubMed Scopus (218) Google Scholar, 80Rull V. Neotropical diversity: timing and potential drivers.Trends Ecol. Evol. 2011; 26: 508-513Abstract Full Text Full Text PDF PubMed Scopus (293) Google Scholar]. These two putative causal factors are not mutually exclusive. Indeed, many studies have found evidence for higher rates of speciation in the tropics [4Krug A.Z. et al.Contrarian clade confirms the ubiquity of spatial origination patterns in the production of latitudinal diversity gradients.Proc. Natl. Acad. Sci. U.S.A. 2007; 104: 18129-18134Crossref PubMed Scopus (33) Google Scholar, 14Krug A.Z. et al.Generation of Earth's first-order biodiversity pattern.Astrobiology. 2009; 9: 113-124Crossref PubMed Scopus (73) Google Scholar, 21Jablonski D. et al.Out of the tropics: evolutionary dynamics of the latitudinal diversity gradient.Science. 2006; 314: 102-106Crossref PubMed Scopus (626) Google Scholar, 44Jablonski D. Extinction and the spatial dynamics of biodiversity.Proc. Natl. Acad. Sci. U.S.A. 2008; 105: 11528-11535Crossref PubMed Scopus (137) Google Scholar, 46Krug A.Z. Patzkowsky M.E. Geographic variation in turnover and recovery from the Late Ordovician mass extinction.Paleobiology. 2007; 33: 435-454Crossref Scopus (43) Google Scholar, 81Allen A.P. Gillooly J.F. Assessing latitudinal gradients in speciation rates and biodiversity at the global scale.Ecol. Lett. 2006; 9: 947-954Crossref PubMed Scopus (168) Google Scholar, 82Allen A.P. et al.Kinetic effects of temperature on rates of genetic divergence and speciation.Proc. Natl. Acad. Sci. U.S.A. 2006; 103: 9130-9135Crossref PubMed Scopus (323) Google Scholar, 83McKenna D.D. Farrell B.D. Tropical forests are both evolutionary cradles and museums of leaf beetle diversity.Proc. Natl. Acad. Sci. U.S.A. 2006; 103: 10947-10951Crossref PubMed Scopus (176) Google Scholar, 84Eo S.H. et al.Population divergence in plant species reflects latitudinal diversity gradients.Biol. Lett. 2008; 4: 382-384Crossref PubMed Scopus (37) Google Scholar, 85Kiessling W. et al.Reefs as cradles of evolution and sources of biodiversity in the Phanerozoic.Science. 2010; 327: 196-198Crossref PubMed Scopus (127) Google Scholar], and a few analyses have demonstrated lower tropical rates of extinction [21Jablonski D. et al.Out of the tropics: evolutionary dynamics of the latitudinal diversity gradient.Science. 2006; 314: 102-106Crossref PubMed Scopus (626) Google Scholar, 23Weir J.T. Schluter D. The latitudinal gradient in recent speciation and extinction rates of birds and mammals.Science. 2007; 315: 1574-1576Crossref PubMed Scopus (414) Google Scholar, 83McKenna D.D. Farrell B.D. Tropical forests are both evolutionary cradles and museums of leaf beetle diversity.Proc. Natl. Acad. Sci. U.S.A. 2006; 103: 10947-10951Crossref PubMed Scopus (176) Google Scholar]. It seems that the tropics might act as both a cradle and museum for biodiversity [21Jablonski D. et al.Out of the tropics: evolutionary dynamics of the latitudinal diversity gradient.Science. 2006; 314: 102-106Crossref PubMed Scopus (626) Google Scholar, 22Mittelbach G.G. et al.Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography.Ecol. Lett. 2007; 10: 315-331Crossref PubMed Scopus (1202) Google Scholar, 83McKenna D.D. Farrell B.D. Tropical forests are both evolutionary cradles and museums of leaf beetle diversity.Proc. Natl. Acad. Sci. U.S.A. 2006; 103: 10947-10951Crossref PubMed Scopus (176) Google Scholar]: Jablonski et al. [21Jablonski D. et al.Out of the tropics: evolutionary dynamics of the latitudinal diversity gradient.Science. 2006; 314: 102-106Crossref PubMed Scopus (626) Google Scholar, 28Jablonski D. et al.Out of the tropics, but how? Fossils, bridge species, and thermal ranges in the dynamics of the marine latitudinal diversity gradient.Proc. Natl. Acad. Sci. U.S.A. 2013; 110: 10487-10494Crossref PubMed Scopus (166) Google Scholar] proposed an 'out of the tropics' model (Figure IC), in which origination rates are higher in the tropics and taxa disperse polewards without losing their tropical presence [14Krug A.Z. et al.Generation of Earth's first-order biodiversity pattern.Astrobiology. 2009; 9: 113-124Crossref PubMed Scopus (73) Google Scholar, 86Valentine J.W. et al.Incumbency, diversity and latitudinal gradients.Paleobiology. 2008; 34: 169-178Crossref Scopus (76) Google Scholar]. However, aspects of all of these models have been questioned: (i) Weir and Schluter [23Weir J.T. Schluter D. The latitudinal gradient in recent speciation and extinction rates of birds and mammals.Science. 2007; 315: 1574-1576Crossref PubMed Scopus (414) Google Scholar] recovered elevated rates of origination at higher latitudes in recent birds and mammals; (ii) higher extinction rates in the tropics were reported for marine invertebrates [24Martin P.R. et al.Revisiting Jablonski (1993): cladogenesis and range expansion explain latitudinal variation in taxonomic richness.J. Evol. Biol. 2007; 20: 930-936Crossref PubMed Scopus (27) Google Scholar] and through simulations [87Arita H.T. Vázquez-Domínguez E. The tropics: cradle, museum or casino? A dynamic null model for latitudinal gradients of species diversity.Ecol. Lett. 2008; 11: 653-663Crossref PubMed Scopus (46) Google Scholar]; (iii) polar extinction rates in bivalves have been found to be lower than temperate rates [13Krug A.Z. et al.Differential extinction and the contrasting structure of polar marine faunas.PLoS ONE. 2010; 5: e15362Crossref PubMed Scopus (28) Google Scholar]; and (iv) other authors have found no evidence for a correlation between diversification rates and latitude at all for a range of groups (e.g., birds, frogs, Foraminifera, and mammals) and through simulation studies [22Mittelbach G.G. et al.Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography.Ecol. Lett. 2007; 10: 315-331Crossref PubMed Scopus (1202) Google Scholar, 27Soria-Carrasco V. Castresana J. Diversification rates and the latitudinal gradient of diversity in mammals.Proc. R. Soc. Lond. B: Biol. Sci. 2012; 279: 4148-4155Crossref Scopus (48) Google Scholar, 88Wiens J.J. et al.Evolutionary and ecological causes of the latitudinal diversity gradient in hylid frogs: tree frogs unearth the roots of high tropical diversity.Am. Nat. 2006; 168: 579-596Crossref PubMed Scopus (351) Google Scholar, 89Escarguel G. et al.Evolutionary rates do not drive latitudinal diversity gradients.J. Zool. Syst. Evol. Res. 2008; 46: 82-86Crossref Scopus (19) Google Scholar, 90Buzas M.A. Culver S.J. Geographic origin of species: the temperate-tropical interchange.Geology. 2009; 37: 879-881Crossref Scopus (8) Google Scholar, 91Jetz W. et al.The global diversity of birds in space and time.Nature. 2012; 491: 444-448Crossref PubMed Scopus (2169) Google Scholar]. Consequently, support for the cradle and museum hypotheses, or some combination of them, is controversial. It is possible that the timing of origination and extinction might have some role, including whether such events occurred during icehouse or greenhouse worlds, or at times of steep or shallow climatic gradients. Clade-specific events might a