Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Perspective
  • Published:

Conceptual and empirical bridges between micro- and macroevolution

Abstract

Explaining broad molecular, phenotypic and species biodiversity patterns necessitates a unifying framework spanning multiple evolutionary scales. Here we argue that although substantial effort has been made to reconcile microevolution and macroevolution, much work remains to identify the links between biological processes at play. We highlight four major questions of evolutionary biology whose solutions require conceptual bridges between micro and macroevolution. We review potential avenues for future research to establish how mechanisms at one scale (drift, mutation, migration, selection) translate to processes at the other scale (speciation, extinction, biogeographic dispersal) and vice versa. We propose ways in which current comparative methods to infer molecular evolution, phenotypic evolution and species diversification could be improved to specifically address these questions. We conclude that researchers are in a better position than ever before to build a synthesis to understand how microevolutionary dynamics unfold over millions of years.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Timescale-dependent rates of molecular evolution, phenotypic evolution and speciation using phylogenetic or fossil data.
Fig. 2: Current and fossil data represent past evolutionary processes incompletely.
Fig. 3: A changing microevolutionary adaptive landscape integrated over a macroevolutionary timescale.

Similar content being viewed by others

References

  1. Huxley, J. Evolution. The Modern Synthesis (George Allen & Unwin, 1942).

  2. Harmon, L. J. et al. Causes and consequences of apparent timescaling across all estimated evolutionary rates. Annu. Rev. Ecol. Evol. Syst. 52, 587–609 (2021).

    Article  Google Scholar 

  3. Charlesworth, B., Lande, R. & Slatkin, M. A neo‐Darwinian commentary on macroevolution. Evolution 36, 474–498 (1982).

    PubMed  Google Scholar 

  4. Estes, S. & Arnold, S. J. Resolving the paradox of stasis: models with stabilizing selection explain evolutionary divergence on all timescales. Am. Nat. 169, 227–244 (2007).

    Article  PubMed  Google Scholar 

  5. Hansen, T. F. & Martins, E. P. Translating between microevolutionary process and macroevolutionary patterns: the correlation structure of interspecific data. Evolution 50, 1404–1417 (1996).

    Article  PubMed  Google Scholar 

  6. Reznick, D. N. & Ricklefs, R. E. Darwin’s bridge between microevolution and macroevolution. Nature 457, 837–842 (2009).

    Article  CAS  PubMed  Google Scholar 

  7. Rolland, J., Silvestro, D., Litsios, G., Faye, L. & Salamin, N. Clownfishes evolution below and above the species level. Proc. R. Soc. B 285, 20171796 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  8. Arnold, S. J., Pfrender, M. E. & Jones, A. G. The adaptive landscape as a conceptual bridge between micro- and macroevolution. Genetica 112, 9–32 (2001).

    Article  PubMed  Google Scholar 

  9. Singhal, S. et al. No link between population isolation and speciation rate in squamate reptiles. Proc. Natl Acad. Sci. USA 119, e2113388119 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  10. Rabosky, D. L. & Matute, D. R. Macroevolutionary speciation rates are decoupled from the evolution of intrinsic reproductive isolation in Drosophila and birds. Proc. Natl Acad. Sci. USA 110, 15354–15359 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Dynesius, M. & Jansson, R. Persistence of within‐species lineages: a neglected control of speciation rates. Evolution 68, 923–934 (2014).

    Article  PubMed  Google Scholar 

  12. Alencar, L. R. V. D. & Quental, T. B. Linking population‐level and microevolutionary processes to understand speciation dynamics at the macroevolutionary scale. Ecol. Evol. 11, 5828–5843 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  13. Hua, X., Herdha, T. & Burden, C. J. Protracted speciation under the state-dependent speciation and extinction approach. Syst. Biol. 71, 1362–1377 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  14. Simpson, G. G. Tempo and Mode in Evolution (Columbia Univ. Press, 1944).

  15. Lewontin, R. C. The Genetic Basis of Evolutionary Change (Columbia Univ. Press, 1974).

  16. Gould, S. J. & Eldredge, N. Punctuated equilibria: the tempo and mode of evolution reconsidered. Paleobiology 3, 115–151 (1977).

    Article  Google Scholar 

  17. Hansen, T. F. & Houle, D. in Phenotypic Integration: Studying the Ecology and Evolution of Complex Phenotypes (eds Pigliucci, M. & Preston, K.) 130–150 (Oxford Univ. Press, 2004).

  18. Haller, B. C. & Hendry, A. P. Solving the paradox of stasis: squashed stabilizing selection and the limits of detection. Evolution 68, 483–500 (2014).

    Article  PubMed  Google Scholar 

  19. Ho, S. Y., Phillips, M. J., Cooper, A. & Drummond, A. J. Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Mol. Biol. Evol. 22, 1561–1568 (2005).

    Article  CAS  PubMed  Google Scholar 

  20. Ho, S. Y. et al. Time‐dependent rates of molecular evolution. Mol. Ecol. 20, 3087–3101 (2011).

    Article  PubMed  Google Scholar 

  21. Ho, S. Y., Duchêne, S., Molak, M. & Shapiro, B. Time‐dependent estimates of molecular evolutionary rates: evidence and causes. Mol. Ecol. 24, 6007–6012 (2015).

    Article  PubMed  Google Scholar 

  22. Gingerich, P. D. Rates of Evolution: a Quantitative Synthesis (Cambridge Univ. Press, 2019).

  23. Magallon, S. & Sanderson, M. J. Absolute diversification rates in angiosperm clades. Evolution 55, 1762–1780 (2001).

    CAS  PubMed  Google Scholar 

  24. Ricklefs, R. E. Evolutionary diversification and the origin of the diversity–environment relationship. Ecology 87, S3–S13 (2006).

    Article  PubMed  Google Scholar 

  25. McPeek, M. A. & Brown, J. M. Clade age and not diversification rate explains species richness among animal taxa. Am. Nat. 169, E97–E106 (2007).

    Article  PubMed  Google Scholar 

  26. Louca, S., Henao‐Diaz, L. F. & Pennell, M. The scaling of diversification rates with age is likely explained by sampling bias. Evolution 76, 1625–1637 (2022).

    Article  PubMed  Google Scholar 

  27. Henao-Diaz, L. F., Harmon, L. J., Sugawara, M. T., Miller, E. T. & Pennell, M. W. Macroevolutionary diversification rates show time dependency. Proc. Natl Acad. Sci. USA 116, 7403–7408 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  28. Yang Z. Computational Molecular Evolution (Oxford Univ. Press, 2006).

  29. Budd, G. E. & Mann, R. P. History is written by the victors: the effect of the push of the past on the fossil record. Evolution 72, 2276–2291 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  30. Nee, S., May, R. M. & Harvey, P. H. The reconstructed evolutionary process. Phil. Trans. R. Soc. Lond. B 344, 305–311 (1994).

    Article  CAS  Google Scholar 

  31. Jablonski, D., Roy, K., Valentine, J. W., Price, R. M. & Anderson, P. S. The impact of the pull of the recent on the history of marine diversity. Science 300, 1133–1135 (2003).

    Article  CAS  PubMed  Google Scholar 

  32. Raup, D. M. Size of the Permo-Triassic bottleneck and its evolutionary implications. Science 206, 217–218 (1979).

    Article  CAS  PubMed  Google Scholar 

  33. Stadler, T. Mammalian phylogeny reveals recent diversification rate shifts. Proc. Natl Acad. Sci. USA 108, 6187–6192 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. O’Meara, B. C. & Beaulieu J. M. Potential survival of some, but not all, diversification methods. Preprint at EcoEvoRxiv https://doi.org/10.32942/osf.io/w5nvd (2022).

  35. Futuyma, D. J. On the role of species in anagenesis. Am. Nat. 130, 465–473 (1987).

    Article  Google Scholar 

  36. Futuyma, D. J. Evolutionary constraint and ecological consequences. Evolution 64, 1865–1884 (2010).

    Article  PubMed  Google Scholar 

  37. Morlon, H., Parsons, T. L. & Plotkin, J. B. Reconciling molecular phylogenies with the fossil record. Proc. Natl Acad. Sci. USA 108, 16327–16332 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Kostikova, A., Silvestro, D., Pearman, P. B. & Salamin, N. Bridging inter- and intraspecific trait evolution with a hierarchical Bayesian approach. Syst. Biol. 65, 417–431 (2016).

    Article  PubMed  Google Scholar 

  39. Gaboriau, T., Mendes, F. K., Joly, S., Silvestro, D. & Salamin, N. A multi‐platform package for the analysis of intra‐ and interspecific trait evolution. Methods Ecol. Evol. 11, 1439–1447 (2020).

    Article  Google Scholar 

  40. Silvestro, D., Salamin, N., Antonelli, A. & Meyer, X. Improved estimation of macroevolutionary rates from fossil data using a Bayesian framework. Paleobiology 45, 546–570 (2019).

    Article  Google Scholar 

  41. Etienne, R. S. & Rosindell, J. Prolonging the past counteracts the pull of the present: protracted speciation can explain observed slowdowns in diversification. Syst. Biol. 61, 204–213 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  42. De Maio, N., Schrempf, D. & Kosiol, C. PoMo: an allele frequency-based approach for species tree estimation. Syst. Biol. 64, 1018–1031 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  43. Slater, G. J., Harmon, L. J. & Alfaro, M. E. Integrating fossils with molecular phylogenies improves inference of trait evolution. Evolution 66, 3931–3944 (2012).

    Article  PubMed  Google Scholar 

  44. Rolland, J. et al. The impact of endothermy on the climatic niche evolution and the distribution of vertebrate diversity. Nat. Ecol. Evol. 2, 459–464 (2018).

    Article  PubMed  Google Scholar 

  45. Silvestro, D., Warnock, R., Gavryushkina, A. & Stadler, T. Closing the gap between palaeontological and neontological speciation and extinction rate estimates. Nat. Commun. 9, 5237 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Mitchell, J. S., Etienne, R. S. & Rabosky, D. L. Inferring diversification rate variation from phylogenies with fossils. Syst. Biol. 68, 1–18 (2019).

    PubMed  Google Scholar 

  47. Černý, D., Madzia, D. & Slater, G. J. Empirical and methodological challenges to the model-based inference of diversification rates in extinct clades. Syst. Biol. 71, 153–171 (2022).

    Article  Google Scholar 

  48. Blois, J. L., Zarnetske, P. L., Fitzpatrick, M. C. & Finnegan, S. Climate change and the past, present, and future of biotic interactions. Science 341, 499–504 (2013).

    Article  CAS  PubMed  Google Scholar 

  49. Duchen, P., Alfaro, M., Rolland, J., Salamin, N. & Silvestro, D. On the effect of asymmetrical trait inheritance on models of trait evolution. Syst. Biol. 70, 376–388 (2021).

    Article  PubMed  Google Scholar 

  50. Voje, K. L., Di Martino, E. & Porto, A. Revisiting a landmark study system: no evidence for a punctuated mode of evolution in Metrarabdotos. Am. Nat. 195, 899–917 (2020).

    Article  PubMed  Google Scholar 

  51. Brombacher, A., Wilson, P. A., Bailey, I. & Ezard, T. H. G. The breakdown of static and evolutionary allometries during climatic upheaval. Evolution 190, 299–450 (2017).

    Google Scholar 

  52. Hunt, G. The relative importance of directional change, random walks, and stasis in the evolution of fossil lineages. Proc. Natl Acad. Sci. USA 104, 18404–18408 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Voje, K. L. Testing eco‐evolutionary predictions using fossil data: phyletic evolution following ecological opportunity. Evolution 74, 188–200 (2020).

    Article  PubMed  Google Scholar 

  54. Webster, M. Morphological homeostasis in the fossil record. Semin. Cell Dev. Biol. 88, 91–104 (2019).

    Article  PubMed  Google Scholar 

  55. Fox, J. W. & Lenski, R. E. From here to eternity—the theory and practice of a really long experiment. PLoS Biol. 13, e1002185 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  56. Fenton, I. S. et al. Triton, a new species-level database of Cenozoic planktonic foraminiferal occurrences. Sci. Data 8, 160 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  57. Fan, J. X. et al. A high-resolution summary of Cambrian to Early Triassic marine invertebrate biodiversity. Science 367, 272–277 (2020).

    Article  CAS  PubMed  Google Scholar 

  58. Lambert, D. M. et al. Rates of evolution in ancient DNA from Adelie penguins. Science 295, 2270–2273 (2002).

    Article  CAS  PubMed  Google Scholar 

  59. Hay, J. M. et al. Rapid molecular evolution in a living fossil. Trends Genet. 24, 106–109 (2008).

    Article  CAS  PubMed  Google Scholar 

  60. Kirch, M., Romundset, A., Gilbert, M. T. P., Jones, F. C. & Foote, A. D. Ancient and modern stickleback genomes reveal the demographic constraints on adaptation. Curr. Biol. 31, 2027–2036 (2021).

    Article  CAS  PubMed  Google Scholar 

  61. Uyeda, J. C., Hansen, T. F., Arnold, S. J. & Pienaar, J. The million-year wait for macroevolutionary bursts. Proc. Natl Acad. Sci. USA 108, 15908–15913 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Landis, M. J. & Schraiber, J. G. Pulsed evolution shaped modern vertebrate body sizes. Proc. Natl Acad. Sci. USA 114, 13224–13229 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Pagel, M., O’Donovan, C. & Meade, A. General statistical model shows that macroevolutionary patterns and processes are consistent with Darwinian gradualism. Nat. Commun. 13, 1113 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Condamine, F. L., Rolland, J. & Morlon, H. Assessing the causes of diversification slowdowns: temperature‐dependent and diversity‐dependent models receive equivalent support. Ecol. Lett. 22, 1900–1912 (2019).

    Article  PubMed  Google Scholar 

  65. Moen, D. & Morlon, H. Why does diversification slow down? Trends Ecol. Evol. 29, 190–197 (2014).

    Article  PubMed  Google Scholar 

  66. Amemiya, C. T. et al. The African coelacanth genome provides insights into tetrapod evolution. Nature 496, 311–316 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Gemmell, N. J. et al. The tuatara genome reveals ancient features of amniote evolution. Nature 584, 403–409 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Zhan, S. H., Otto, S. P. & Barker, M. S. Broad variation in rates of polyploidy and dysploidy across flowering plants is correlated with lineage diversification. Preprint at bioRxiv https://doi.org/10.1101/2021.03.30.436382 (2021).

  69. Merilä, J. & Crnokrak, P. Comparison of genetic differentiation at marker loci and quantitative traits. J. Evol. Biol. 14, 892–903 (2001).

    Article  Google Scholar 

  70. Merilä, J. & Hendry, A. P. Climate change, adaptation, and phenotypic plasticity: the problem and the evidence. Evol. Appl. 7, 1–14 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  71. Pujol, B. et al. The missing response to selection in the wild. Trends Ecol. Evol. 33, 337–346 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  72. Bonnet, T. et al. Genetic variance in fitness indicates rapid contemporary adaptive evolution in wild animals. Science 376, 1012–1016 (2022).

    Article  CAS  PubMed  Google Scholar 

  73. Bonamour, S., Teplitsky, C., Charmantier, A., Crochet, P. A. & Chevin, L. M. Selection on skewed characters and the paradox of stasis. Evolution 71, 2703–2713 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  74. Schluter, D. & Grant, P. R. Determinants of morphological patterns in communities of Darwin’s finches. Am. Nat. 123, 175–196 (1984).

    Article  Google Scholar 

  75. Voje, K. L. Tempo does not correlate with mode in the fossil record. Evolution 70, 2678–2689 (2016).

    Article  PubMed  Google Scholar 

  76. Mustonen, V. & Lässig, M. From fitness landscapes to seascapes: non-equilibrium dynamics of selection and adaptation. Trends Genet. 25, 111–119 (2009).

    Article  CAS  PubMed  Google Scholar 

  77. Payne, J. L. & Wagner, A. The causes of evolvability and their evolution. Nat. Rev. Genet. 20, 24–38 (2019).

    Article  CAS  PubMed  Google Scholar 

  78. Hansen, T. F. in The Adaptive Landscape in Evolutionary Biology (eds Svensson, E. & Calsbeek, R.) Ch. 13 (Oxford Univ. Press, 2013).

  79. Rolland, J., Jiguet, F., Jønsson, K. A., Condamine, F. L. & Morlon, H. Settling down of seasonal migrants promotes bird diversification. Proc. R. Soc. B 281, 20140473 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  80. Zanne, A. E. et al. Three keys to the radiation of angiosperms into freezing environments. Nature 506, 89–92 (2014).

    Article  CAS  PubMed  Google Scholar 

  81. Hirt, M. R., Jetz, W., Rall, B. C. & Brose, U. A general scaling law reveals why the largest animals are not the fastest. Nat. Ecol. Evol. 1, 1116–1122 (2017).

    Article  PubMed  Google Scholar 

  82. Araújo, M. B. et al. Heat freezes niche evolution. Ecol. Lett. 16, 1206–1219 (2013).

    Article  PubMed  Google Scholar 

  83. Martin, C. H. & Wainwright, P. C. Multiple fitness peaks on the adaptive landscape drive adaptive radiation in the wild. Science 339, 208–211 (2013).

    Article  CAS  PubMed  Google Scholar 

  84. Schluter, D. Adaptive radiation along genetic lines of least resistance. Evolution 50, 1766–1774 (1996).

    Article  PubMed  Google Scholar 

  85. Butler, M. A. & King, A. A. Phylogenetic comparative analysis: a modeling approach for adaptive evolution. Am. Nat. 164, 683–695 (2004).

    Article  PubMed  Google Scholar 

  86. Boucher, F. C. & Démery, V. Inferring bounded evolution in phenotypic characters from phylogenetic comparative data. Syst. Biol. 65, 651–661 (2016).

    Article  PubMed  Google Scholar 

  87. Mahler, D. L., Ingram, T., Revell, L. J. & Losos, J. B. Exceptional convergence on the macroevolutionary landscape in island lizard radiations. Science 341, 292–295 (2013).

    Article  CAS  PubMed  Google Scholar 

  88. FitzJohn, R. G. Quantitative traits and diversification. Syst. Biol. 59, 619–633 (2010).

    Article  PubMed  Google Scholar 

  89. Gould, S. J. Gulliver’s further travels: the necessity and difficulty of a hierarchical theory of selection. Phil. Trans. R. Soc. Lond. B 353, 307–314 (1998).

    Article  CAS  Google Scholar 

  90. Rabosky, D. L. & McCune, A. R. Reinventing species selection with molecular phylogenies. Trends Ecol. Evol. 25, 68–74 (2010).

    Article  PubMed  Google Scholar 

  91. Martins, M. J. F., Puckett, T. M., Lockwood, R., Swaddle, J. P. & Hunt, G. High male sexual investment as a driver of extinction in fossil ostracods. Nature 556, 366–369 (2018).

    Article  CAS  PubMed  Google Scholar 

  92. McGlothlin, J. W. et al. Adaptive radiation along a deeply conserved genetic line of least resistance in Anolis lizards. Evol. Lett. 2, 310–322 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  93. Houle, D., Bolstad, G. H., van der Linde, K. & Hansen, T. F. Mutation predicts 40 million years of fly wing evolution. Nature 548, 447–450 (2017).

    Article  CAS  PubMed  Google Scholar 

  94. Zalts, H. & Yanai, I. Developmental constraints shape the evolution of the nematode mid-developmental transition. Nat. Ecol. Evol. 1, 0113 (2017).

    Article  Google Scholar 

  95. Pennell, M. W., Harmon, L. J. & Uyeda, J. C. Is there room for punctuated equilibrium in macroevolution? Trends Ecol. Evol. 29, 23–32 (2014).

    Article  PubMed  Google Scholar 

  96. Hunt, G. Testing the link between phenotypic evolution and speciation: an integrated palaeontological and phylogenetic analysis. Methods Ecol. Evol. 4, 714–723 (2013).

    Article  Google Scholar 

  97. Schluter, D. The Ecology of Adaptive Radiation (OUP, 2000).

  98. Rabosky, D. L. et al. Rates of speciation and morphological evolution are correlated across the largest vertebrate radiation. Nat. Commun. 4, 1958 (2013).

    Article  PubMed  Google Scholar 

  99. Erwin, D. H., Valentine, J. W. & Sepkoski, J. J. A comparative study of diversification events: the early Paleozoic versus the Mesozoic. Evolution 41, 1177–1186 (1987).

    Article  CAS  PubMed  Google Scholar 

  100. Parins-Fukuchi, C., Stull, G. W. & Smith, S. A. Phylogenomic conflict coincides with rapid morphological innovation. Proc. Natl Acad. Sci. USA 118, e2023058118 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Stull, G. W. et al. Gene duplications and phylogenomic conflict underlie major pulses of phenotypic evolution in gymnosperms. Nat. Plants 7, 1015–1025 (2021).

    Article  PubMed  Google Scholar 

  102. Schluter, D. & Rieseberg, L. H. Three problems in the genetics of speciation by selection. Proc. Natl Acad. Sci. USA 119, e2122153119 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Anderson, S. A. & Weir, J. T. Character displacement drives trait divergence in a continental fauna. Proc. Natl Acad. Sci. USA 118, e2021209118 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Germain, R. M. et al. On the origin of coexisting species. Trends Ecol. Evol. 36, 284–293 (2021).

    Article  PubMed  Google Scholar 

  105. Venditti, C. & Pagel, M. Speciation as an active force in promoting genetic evolution. Trends Ecol. Evol. 25, 14–20 (2010).

    Article  PubMed  Google Scholar 

  106. Coyne, J. A. & Orr, H. A. Speciation (Sinauer, 2004).

  107. Rundell, R. J. & Price, T. D. Adaptive radiation, nonadaptive radiation, ecological speciation and nonecological speciation. Trends Ecol. Evol. 24, 394–399 (2009).

    Article  PubMed  Google Scholar 

  108. Rabosky, D. L. Phylogenetic tests for evolutionary innovation: the problematic link between key innovations and exceptional diversification. Phil. Trans. R. Soc. Lond. B 372, 20160417 (2017).

    Article  Google Scholar 

  109. Lanfear, R., Ho, S. Y., Love, D. & Bromham, L. Mutation rate is linked to diversification in birds. Proc. Natl Acad. Sci. USA 107, 20423–20428 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Dowle, E. J., Morgan-Richards, M. & Trewick, S. A. Molecular evolution and the latitudinal biodiversity gradient. Heredity 110, 501–510 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. & West, G. B. Toward a metabolic theory of ecology. Ecology 85, 1771–1789 (2004).

    Article  Google Scholar 

  112. Orton, M. G., May, J. A., Ly, W., Lee, D. J. & Adamowicz, S. J. Is molecular evolution faster in the tropics? Heredity 122, 513–524 (2019).

    Article  CAS  PubMed  Google Scholar 

  113. Hull, P. M. & Norris, R. D. Evidence for abrupt speciation in a classic case of gradual evolution. Proc. Natl Acad. Sci. USA 106, 21224–21229 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Franks, S. J., Hamann, E. & Weis, A. E. Using the resurrection approach to understand contemporary evolution in changing environments. Evol. Appl. 11, 17–28 (2018).

    Article  PubMed  Google Scholar 

  115. Goldberg, E. E. & Igić, B. Tempo and mode in plant breeding system evolution. Evolution 66, 3701–3709 (2012).

    Article  PubMed  Google Scholar 

  116. Wright, A. M., Bapst, D. W., Barido-Sottani, J. & Warnock, R. C. Integrating fossil observations into phylogenetics using the fossilized birth–death model. Annu. Rev. Ecol. Evol. Syst. 53, 251–273 (2022).

    Article  Google Scholar 

  117. Manceau, M., Marin, J., Morlon, H. & Lambert, A. Model-based inference of punctuated molecular evolution. Mol. Biol. Evol. 37, 3308–3323 (2020).

    Article  CAS  PubMed  Google Scholar 

  118. Obermeyer, F. et al. Analysis of 6.4 million SARS-CoV-2 genomes identifies mutations associated with fitness. Science 376, 1327–1332 (2022).

    Article  CAS  PubMed  Google Scholar 

  119. Weber, M. G., Wagner, C. E., Best, R. J., Harmon, L. J. & Matthews, B. Evolution in a community context: on integrating ecological interactions and macroevolution. Trends Ecol. Evol. 32, 291–304 (2017).

    Article  PubMed  Google Scholar 

  120. Aristide, L. & Morlon, H. Understanding the effect of competition during evolutionary radiations: an integrated model of phenotypic and species diversification. Ecol. Lett. 22, 2006–2017 (2019).

    Article  PubMed  Google Scholar 

  121. Nuismer, S. L. & Harmon, L. J. Predicting rates of interspecific interaction from phylogenetic trees. Ecol. Lett. 18, 17–27 (2015).

    Article  PubMed  Google Scholar 

  122. Harmon, L. J. et al. Detecting the macroevolutionary signal of species interactions. J. Evol. Biol. 32, 769–782 (2019).

    Article  PubMed  Google Scholar 

  123. Blasco-Costa, I., Hayward, A., Poulin, R. & Balbuena, J. A. Next-generation cophylogeny: unravelling eco-evolutionary processes. Trends Ecol. Evol. 36, 907–918 (2021).

    Article  PubMed  Google Scholar 

  124. Hembry, D. H. & Weber, M. G. Ecological interactions and macroevolution: a new field with old roots. Annu. Rev. Ecol. Evol. Syst. 51, 215–243 (2020).

    Article  Google Scholar 

  125. Phillimore, A. B. & Price, T. D. Density-dependent cladogenesis in birds. PLoS Biol. 6, e71 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  126. Morlon, H., Potts, M. D. & Plotkin, J. B. Inferring the dynamics of diversification: a coalescent approach. PLoS Biol. 8, e1000493 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  127. Liow, L. H., Reitan, T. & Harnik, P. G. Ecological interactions on macroevolutionary time scales: clams and brachiopods are more than ships that pass in the night. Ecol. Lett. 18, 1030–1039 (2015).

    Article  PubMed  Google Scholar 

  128. Silvestro, D., Antonelli, A., Salamin, N. & Quental, T. B. The role of clade competition in the diversification of North American canids. Proc. Natl Acad. Sci. USA 112, 8684–8689 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Condamine, F. L., Silvestro, D., Koppelhus, E. B. & Antonelli, A. The rise of angiosperms pushed conifers to decline during global cooling. Proc. Natl Acad. Sci. USA 117, 28867–28875 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Harmon, L. J. & Harrison, S. Species diversity is dynamic and unbounded at local and continental scales. Am. Nat. 185, 584–593 (2015).

    Article  PubMed  Google Scholar 

  131. Rabosky, D. L. & Hurlbert, A. H. Species richness at continental scales is dominated by ecological limits. Am. Nat. 185, 572–583 (2015).

    Article  PubMed  Google Scholar 

  132. Etienne, R. S. et al. Diversity-dependence brings molecular phylogenies closer to agreement with the fossil record. Proc. R. Soc. B 279, 1300–1309 (2012).

    Article  PubMed  Google Scholar 

  133. Etienne, R. S. & Haegeman, B. A conceptual and statistical framework for adaptive radiations with a key role for diversity dependence. Am. Nat. 180, E75–E89 (2012).

    Article  PubMed  Google Scholar 

  134. Rabosky, D. L. Diversity-dependence, ecological speciation, and the role of competition in macroevolution. Annu. Rev. Ecol. Evol. Syst. 44, 481–502 (2013).

    Article  Google Scholar 

  135. Harmon, L. J., Schulte, J. A., Larson, A. & Losos, J. B. Tempo and mode of evolutionary radiation in iguanian lizards. Science 301, 961–964 (2003).

    Article  CAS  PubMed  Google Scholar 

  136. Tobias, J. A. et al. Species coexistence and the dynamics of phenotypic evolution in adaptive radiation. Nature 506, 359–363 (2014).

    Article  CAS  PubMed  Google Scholar 

  137. Drury, J. P. et al. Tempo and mode of morphological evolution are decoupled from latitude in birds. PLoS Biol. 19, e3001270 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Carvalho, M. R. et al. Extinction at the end-Cretaceous and the origin of modern Neotropical rainforests. Science 372, 63–68 (2021).

    Article  CAS  PubMed  Google Scholar 

  139. Reitan, T., Schweder, T. & Henderiks, J. Phenotypic evolution studied by layered stochastic differential equations. Ann. Appl. Stat. 6, 1531–1551 (2012).

    Article  Google Scholar 

  140. Xu, L., Van Doorn, S., Hildenbrandt, H. & Etienne, R. S. Inferring the effect of species interactions on trait evolution. Syst. Biol. 70, 463–479 (2021).

    Article  PubMed  Google Scholar 

  141. Tóth, A. B. et al. Reorganization of surviving mammal communities after the end-Pleistocene megafaunal extinction. Science 365, 1305–1308 (2019).

    Article  PubMed  Google Scholar 

  142. Luo, M., Ji, Y., Warton, D. & Yu, D. W. Extracting abundance information from DNA‐based data. Mol. Ecol. Resour. 23, 174–189 (2023).

    Article  CAS  PubMed  Google Scholar 

  143. Li, H. & Durbin, R. Inference of human population history from individual whole-genome sequences. Nature 475, 493–496 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Ferriere, R. & Legendre, S. Eco-evolutionary feedbacks, adaptive dynamics and evolutionary rescue theory. Phil. Trans. R. Soc. Lond. B 368, 20120081 (2013).

    Article  Google Scholar 

  145. Odling-Smee, F. J., Laland, K. N., & Feldman, M. W. Niche Construction: The Neglected Process in Evolution (Princeton Univ. Press, 2013).

  146. Arditti, J., Elliott, J., Kitching, I. J. & Wasserthal, L. T. ‘Good Heavens what insect can suck it’—Charles Darwin, Angraecum sesquipedale and Xanthopan morganii praedicta. Bot. J. Linn. Soc. 169, 403–432 (2012).

    Article  Google Scholar 

  147. Harvey, M. G. et al. Positive association between population genetic differentiation and speciation rates in New World birds. Proc. Natl Acad. Sci. USA 114, 6328–6333 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Freeman, B. G., Strimas-Mackey, M. & Miller, E. T. Interspecific competition limits bird species’ ranges in tropical mountains. Science 377, 416–420 (2022).

    Article  CAS  PubMed  Google Scholar 

  149. FitzJohn, R. G. Diversitree: comparative phylogenetic analyses of diversification in R. Methods Ecol. Evol. 3, 1084–1092 (2012).

    Article  Google Scholar 

  150. Freeman, B. G., Rolland, J., Montgomery, G. A. & Schluter, D. Faster evolution of a premating reproductive barrier is not associated with faster speciation rates in New World passerine birds. Proc. R. Soc. B 289, 20211514 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  151. Rolland, J., Schluter, D. & Romiguier, J. Vulnerability to fishing and life history traits correlate with the load of deleterious mutations in teleosts. Mol. Biol. Evol. 37, 2192–2196 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Ogbunugafor, C. B., Wylie, C. S., Diakite, I., Weinreich, D. M. & Hartl, D. L. Adaptive landscape by environment interactions dictate evolutionary dynamics in models of drug resistance. PLoS Comput. Biol. 12, e1004710 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  153. Lewontin, R. C. The units of selection. Annu. Rev. Ecol. Evol. Syst. 1, 1–18 (1970).

    Article  Google Scholar 

  154. Pimiento, C. et al. Selective extinction against redundant species buffers functional diversity. Proc. R. Soc. B 287, 20201162 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  155. Vrba, E. S. & Gould, S. J. The hierarchical expansion of sorting and selection: sorting and selection cannot be equated. Paleobiology 12, 217–228 (1986).

    Article  Google Scholar 

  156. Erwin, D. H. Macroevolution is more than repeated rounds of microevolution. Evol. Dev. 2, 78–84 (2000).

    Article  CAS  PubMed  Google Scholar 

  157. Gould, S. J. Wonderful Life: The Burgess Shale and the Nature of History (WW Norton & Company, 1989).

  158. Blount, Z. D., Lenski, R. E. & Losos, J. B. Contingency and determinism in evolution: replaying life’s tape. Science 362, eaam5979 (2018).

    Article  PubMed  Google Scholar 

  159. Grant, P. R. & Grant, B. R. Unpredictable evolution in a 30-year study of Darwin’s finches. Science 296, 707–711 (2002).

    Article  CAS  PubMed  Google Scholar 

  160. Uyeda, J. C., Zenil-Ferguson, R. & Pennell, M. W. Rethinking phylogenetic comparative methods. Syst. Biol. 67, 1091–1109 (2018).

    Article  PubMed  Google Scholar 

  161. Li, J., Huang, J. P., Sukumaran, J. & Knowles, L. L. Microevolutionary processes impact macroevolutionary patterns. BMC Evol. Biol. 18, 123 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This Perspective was designed during the working group ‘Linking micro and macroevolution’ organized by J.R. with advice from D. Schluter at the University of British Columbia (UBC). Funding was provided to J.R. through a UBC grant for Catalyzing Biodiversity research. We thank K. Beall and L. Rieseberg for their support of this meeting. J.R. also received funding from the European Union’s Horizon 2020 Research and Innovation programme under Marie Skłodowska-Curie grant no. 785910 and from Investissement d’Avenir grants managed by the Agence Nationale de la Recherche (CEBA: ANR-10-LABX-25– 01; TULIP: ANR-10-LABX-0041). M.D., R.G., J.E.M., S.P.O., M.P. and D. Schluter received grant support from the Natural Sciences and Engineering Research Council of Canada (Discovery Grant). D. Silvestro received funding from the Swiss National Science Foundation (PCEFP3_187012), the Swedish Research Council (VR: 2019-04739) and the Foundation for Environmental Strategic Research, Sweden (BIOPATH). A.M. was funded by the Charles University Research Centre programme (no. 204069), the StGACR 23-05977S Czech Science Foundation and the European Union’s Horizon 2020 Research and Innovation programme under Marie Sklodowska-Curie grant no. 785799. L.H.L. received funding from the European Research Council under the European Union’s Horizon 2020 Research and Innovation programme (grant agreement no. 724324). C.E.W. was partially supported by US National Science Foundation grant DEB-1556963.

Author information

Authors and Affiliations

Authors

Contributions

J.R., L.F.H.-D., M.D., R.G., L.J.H., L.L.K., L.H.L., J.E.M., A.M., S.P.O., M.P., N.S., D. Silvestro, M.S., J.U., C.E.W. and D. Schluter participated in the workshop and designed the research. J.R. wrote the first draft. All co-authors participated in commenting and editing the paper, with substantial contribution from J.R. and D. Schluter.

Corresponding author

Correspondence to Jonathan Rolland.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Ecology & Evolution thanks Leonie Moyle and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rolland, J., Henao-Diaz, L.F., Doebeli, M. et al. Conceptual and empirical bridges between micro- and macroevolution. Nat Ecol Evol 7, 1181–1193 (2023). https://doi.org/10.1038/s41559-023-02116-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-023-02116-7

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing