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Historical warming consistently decreased size, dispersal and speciation rate of fish

Nature Climate Change volume 11, pages 787–793 (2021)Cite this article

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Abstract

There is ongoing debate as to whether fish body size will decrease with global warming and how these changes may impact dispersal ability and speciation rate. Theory predicts that, under warmer temperatures, fish grow to a smaller size, undergo a reduction in dispersal ability and increase speciation rates. However, evaluations of such predictions are hampered owing to the lack of empirical data spanning both wide temporal and geographical scales. Here, using phylogenetic methods, we show that smaller clupeiform fish (anchovies and herrings) occurred historically in warmer waters, moved the shortest distances at low speed and displayed the lowest speciation rates. Furthermore, fish moved faster and evolved rapidly under higher rates of temperature change but these historical rates are far lower than current warming rates. Our results predict a future where smaller clupeiform fish that have reduced ability to move will be more prevalent; this, in turn, may reduce future speciation.

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Fig. 1: Global warming can impact fish species in multiple ways.
Fig. 2: Clupeiformes evolved smaller size in warmer temperatures for millions of years and in recent times.
Fig. 3: The ancestor of Clupeoidei was distributed across the eastern Proto Atlantic Ocean and the western Tethys Ocean, 111 Ma.
Fig. 4: Fish dispersal ability depends on body size.
Fig. 5: Clupeiformes moved faster and have evolved rapidly when temperature changed at higher rates.
Fig. 6: Clupeiformes with lower dispersal abilities have lower probabilities of originating new species.

Data availability

The dataset analysed during this study is available from the Dryad repository https://doi.org/10.5061/dryad.cfxpnvx5g.

Code availability

All analyses in this study were done using BayesTraits v.3 available at http://www.evolution.rdg.ac.uk/SoftwareMain.html.

References

  1. Parmesan, C. Ecological and evolutionary responses to recent climate change. Annu. Rev. Ecol. Evol. Syst. 37, 637–669 (2006).

    Article  Google Scholar 

  2. Sheridan, J. A. & Bickford, D. Shrinking body size as an ecological response to climate change. Nat. Clim. Change 1, 401–406 (2011).

    Article  Google Scholar 

  3. Gardner, J. L., Peters, A., Kearney, M. R., Joseph, L. & Heinsohn, R. Declining body size: a third universal response to warming? Trends Ecol. Evol. 26, 285–291 (2011).

    Article  Google Scholar 

  4. McCauley, S. J. & Mabry, K. E. Climate change, body size, and phenotype dependent dispersal. Trends Ecol. Evol. 26, 554–555 (2011).

    Article  Google Scholar 

  5. Norberg, J., Urban, M. C., Vellend, M., Klausmeier, C. A. & Loeuille, N. Eco-evolutionary responses of biodiversity to climate change. Nat. Clim. Change 2, 747–751 (2012).

    Article  Google Scholar 

  6. Amigo, I. The Amazon’s fragile future. Nature 578, 505–507 (2020).

    Article  CAS  Google Scholar 

  7. Reddin, C. J., Nätscher, P. S., Kocsis, Á. T., Pörtner, H. O. & Kiessling, W. Marine clade sensitivities to climate change conform across timescales. Nat. Clim. Change 10, 249–253 (2020).

    Article  Google Scholar 

  8. Comte, L. & Olden, J. D. Climatic vulnerability of the world’s freshwater and marine fishes. Nat. Clim. Change 7, 718–722 (2017).

    Article  Google Scholar 

  9. Skelly, D. K. et al. Evolutionary responses to climate change. Conserv. Biol. 21, 1353–1355 (2007).

    Article  Google Scholar 

  10. Chen, I., Hill, J. K., Ohlemûller, R., Roy, D. B. & Thomas, C. D. Rapid range shifts of species associated with high levels of climate warming. Science 333, 1024–1026 (2011).

    Article  CAS  Google Scholar 

  11. Cheung, W. W. L. et al. Projecting global marine biodiversity impacts under climate change scenarios. Fish Fish. 10, 235–251 (2009).

    Article  Google Scholar 

  12. Cheung, W. W. L. et al. Shrinking of fishes exacerbates impacts of global ocean changes on marine ecosystems. Nat. Clim. Change 3, 254–258 (2013).

    Article  Google Scholar 

  13. Crozier, L. G. & Hutchings, J. A. Plastic and evolutionary responses to climate change in fish. Evol. Appl. 7, 68–87 (2014).

    Article  Google Scholar 

  14. Travis, J. M. J. et al. Dispersal and species’ responses to climate change. Oikos 122, 1532–1540 (2013).

    Article  Google Scholar 

  15. Pauly, D. & Cheung, W. W. L. Sound physiological knowledge and principles in modeling shrinking of fishes under climate change. Glob. Change Biol. 24, e15–e26 (2018).

    Article  Google Scholar 

  16. Tamario, C., Sunde, J., Petersson, E., Tibblin, P. & Forsman, A. Ecological and evolutionary consequences of environmental change and management actions for migrating fish. Front. Ecol. Evol. 7, 271 (2019).

    Article  Google Scholar 

  17. Ljungström, G., Claireaux, M., Fiksen, Ø. & Jørgensen, C. Body size adaptions under climate change: zooplankton community more important than temperature or food abundance in model of a zooplanktivorous fish. Mar. Ecol. Prog. Ser. 636, 1–18 (2020).

    Article  CAS  Google Scholar 

  18. Daufresne, M., Lengfellner, K. & Sommer, U. Global warming benefits the small in aquatic ecosystems. Proc. Natl Acad. Sci. USA 106, 12788–12793 (2009).

    Article  CAS  Google Scholar 

  19. Lenoir, J. et al. Species better track climate warming in the oceans than on land. Nat. Ecol. Evol. 4, 1044–1059 (2020).

    Article  Google Scholar 

  20. Audzijonyte, A. et al. Fish body sizes change with temperature but not all species shrink with warming. Nat. Ecol. Evol. 4, 809–814 (2020).

    Article  Google Scholar 

  21. Rosenzweig, M. L. Loss of speciation rate will impoverish future diversity. Proc. Natl Acad. Sci. USA 98, 5404–5410 (2001).

    Article  CAS  Google Scholar 

  22. Burns, M. D. & Bloom, D. D. Migratory lineages rapidly evolve larger body sizes than non-migratory relatives in ray-finned fishes. Proc. Biol. Sci. 287, 20192615 (2020).

    Google Scholar 

  23. Comte, L. & Olden, J. D. Evidence for dispersal syndromes in freshwater fishes. Proc. R. Soc. B 285, 20172214 (2018).

    Article  Google Scholar 

  24. Bohonak, A. J. Dispersal, gene flow, and population structure. Q. Rev. Biol. 74, 21–45 (1999).

    Article  CAS  Google Scholar 

  25. Perry, A. L., Low, P. J., Ellis, J. R. & Reynolds, J. D. Climate change and distribution shifts in marine fishes. Science 308, 1912–1915 (2005).

    Article  CAS  Google Scholar 

  26. Pinsky, M. L., Worm, B., Fogarty, M. J., Sarmiento, J. L. & Levin, S. A. Marine taxa track local climate velocities. Science 341, 1239–1242 (2013).

    Article  CAS  Google Scholar 

  27. Stevens, V. M. et al. A comparative analysis of dispersal syndromes in terrestrial and semi-terrestrial animals. Ecol. Lett. 17, 1039–1052 (2014).

    Article  Google Scholar 

  28. Dieckmann, U., O’Hara, B. & Weisser, W. The evolutionary ecology of dispersal. Trends Ecol. Evol. 14, 88–90 (1999).

    Article  Google Scholar 

  29. Kokko, H. & López-Sepulcre, A. From individual dispersal to species ranges: perspectives for a changing world. Science 313, 789–791 (2006).

    Article  CAS  Google Scholar 

  30. Lavoué, S., Miya, M., Musikasinthorn, P., Chen, W. J. & Nishida, M. Mitogenomic evidence for an indo-west Pacific origin of the Clupeoidei (Teleostei: Clupeiformes). PLoS ONE 8, e56485 (2013).

    Article  CAS  Google Scholar 

  31. Bloom, D. D., Burns, M. D. & Schriever, T. A. Evolution of body size and trophic position in migratory fishes: a phylogenetic comparative analysis of Clupeiformes (anchovies, herring, shad and allies). Biol. J. Linn. Soc. 125, 302–314 (2018).

    Article  Google Scholar 

  32. O’Donovan, C., Meade, A. & Venditti, C. Dinosaurs reveal the geographical signature of an evolutionary radiation. Nat. Ecol. Evol. 2, 452–458 (2018).

    Article  Google Scholar 

  33. Cheng, L. et al. Record-setting ocean warmth continued in 2019. Adv. Atmos. Sci. 37, 137–142 (2020).

    Article  Google Scholar 

  34. Pinek, L., Mansour, I., Lakovic, M., Ryo, M. & Rillig, M. C. Rate of environmental change across scales in ecology. Biol. Rev. 95, 1798–1811 (2020).

    Article  Google Scholar 

  35. Avaria-Llautureo, J., Hernández, C. E., Rodríguez-Serrano, E. & Venditti, C. The decoupled nature of basal metabolic rate and body temperature in endotherm evolution. Nature 572, 651–654 (2019).

    Article  CAS  Google Scholar 

  36. Gaston, K. J. Species-range size distributions: products of speciation, extinction and transformation. Philos. Trans. R. Soc. B 353, 219–230 (1998).

    Article  Google Scholar 

  37. Baker, J., Meade, A., Pagel, M. & Venditti, C. Positive phenotypic selection inferred from phylogenies. Biol. J. Linn. Soc. 118, 95–115 (2016).

    Article  Google Scholar 

  38. Angilletta, M. J. & Dunham, A. E. The temperature–size rule in ectotherms: simple evolutionary explanations may not be general. Am. Nat. 162, 332–342 (2003).

    Article  Google Scholar 

  39. Quintero, I. & Wiens, J. J. Rates of projected climate change dramatically exceed past rates of climatic niche evolution among vertebrate species. Ecol. Lett. 16, 1095–1103 (2013).

    Article  Google Scholar 

  40. Pauly, D., Christensen, V., Dalsgaard, J., Froese, R. & Torres, F. Jr Fishing down marine food webs. Science 279, 860–863 (1998).

    Article  CAS  Google Scholar 

  41. Rabosky, D. L. et al. An inverse latitudinal gradient in speciation rate for marine fishes. Nature 559, 392–395 (2018).

    Article  CAS  Google Scholar 

  42. Whitehead, P. J. P. FAO species catalogue: vol. 7 Clupeoid fishes of the world. FAO Fish. Synop. 7, 303 (1985).

    Google Scholar 

  43. Charnov, E. L. & Berrigan, D. Evolution of life history parameters in animals with indeterminate growth, particularly fish. Evol. Ecol. 5, 63–68 (1991).

    Article  Google Scholar 

  44. Önsoy, B., Tarkan, A. S., Filiz, H. & Bilge, G. Determination of the best length measurement of fish. North. West. J. Zool. 7, 178–180 (2011).

    Google Scholar 

  45. Mohseni, O. & Stefan, H. G. Stream temperature/air temperature relationship: a physical interpretation. J. Hydrol. 218, 128–141 (1999).

    Article  Google Scholar 

  46. Morrill, J. C., Bales, R. C. & Conklin, M. H. Estimating stream temperature from air temperature: implications for future water quality. J. Environ. Eng. 131, 139–146 (2005).

    Article  CAS  Google Scholar 

  47. Sharma, S., Jackson, D. A., Minns, C. K. & Shuter, B. J. Will northern fish populations be in hot water because of climate change? Glob. Change Biol. 13, 2052–2064 (2007).

    Article  Google Scholar 

  48. Avaria-Llautureo, J. et al. Data for: Historical Warming Consistently Decreased Size, Dispersal and Speciation Rate of Fish (Dryad, 2021); https://doi.org/10.5061/dryad.cfxpnvx5g

  49. Pagel, M., Meade, A. & Barker, D. Bayesian estimation of ancestral character states on phylogenies. Syst. Biol. 53, 673–684 (2004).

    Article  Google Scholar 

  50. Venditti, C., Meade, A. & Pagel, M. Multiple routes to mammalian diversity. Nature 479, 393–396 (2011).

    Article  CAS  Google Scholar 

  51. Kocsis, Á. T. & Raja, N. B. chronosphere (Zenodo, 2020); https://doi.org/10.5281/zenodo.3530703

  52. Raftery, A. E. in Markov Chain Monte Carlo in Practice (eds Gilks, W. et al.) 163–187 (Chapman & Hall, 1996).

  53. Hijmans, R. J. geosphere: spherical trigonometry. R package version 1.5-10 https://CRAN.R-project.org/package=geosphere (2019).

  54. Harvey, M. G. & Rabosky, D. L. Continuous traits and speciation rates: alternatives to state-dependent diversification models. Methods Ecol. Evol. 9, 984–993 (2018).

    Article  Google Scholar 

  55. Title, P. O. & Rabosky, D. L. Tip rates, phylogenies and diversification: what are we estimating, and how good are the estimates? Methods Ecol. Evol. 10, 821–834 (2019).

    Article  Google Scholar 

  56. Louca, S. & Pennell, M. W. Extant timetrees are consistent with a myriad of diversification histories. Nature 580, 502–505 (2020).

    Article  CAS  Google Scholar 

  57. Shafir, A., Azouri, D., Goldberg, E. E. & Mayrose, I. Heterogeneity in the rate of molecular sequence evolution substantially impacts the accuracy of detecting shifts in diversification rates. Evolution 74, 1620–1639 (2020).

    Article  Google Scholar 

  58. Ganzach, Y. Misleading interaction and curvilinear terms. Psychol. Methods 2, 235–247 (1997).

    Article  Google Scholar 

  59. Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).

    Article  Google Scholar 

  60. Lunt, D. J. et al. Palaeogeographic controls on climate and proxy interpretation. Clim. Past 12, 1181–1198 (2016).

    Article  Google Scholar 

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Acknowledgements

We thank C. O’Donovan for her help and advice with the Geo model analyses and A. Meade for data analysis with the computer cluster at University of Reading. We thank D. D. Bloom who shared data of Clupeiformes. ANID FONDECYT postdoctoral grant no. 3200654 supported J.A.-L. ANID FONDECYT initiation grant no. 11180897 and Nucleo Milenio INVASAL funded by ANID – Millennium Science Initiative – NCN16_034 supported C.B.C.-A. The Leverhulme Trust Research Project grant (RPG-2017-071) and a Leverhulme Trust Research Leadership Award (RL-2019-012) supported C.V. ANID FONDECYT regular grant no. 1200843 supported M.M.R. ANID FONDECYT regular grant nos 1201506 and 1170815 supported J.A.-L., C.E.H. and R.J.R.

Author information

Authors and Affiliations

  1. Centro de Estudios Avanzados en Zonas Áridas, CEAZA, Coquimbo, Chile

    Jorge Avaria-Llautureo & Marcelo M. Rivadeneira

  2. School of Biological Sciences, University of Reading, Reading, UK

    Chris Venditti

  3. Departamento de Biología Marina, Facultad de Ciencias del Mar, Universidad Católica del Norte, Coquimbo, Chile

    Marcelo M. Rivadeneira

  4. Departamento de Biología, Universidad de La Serena, La Serena, Chile

    Marcelo M. Rivadeneira

  5. Laboratorio de Ecología Evolutiva y Filoinformática, Departamento de Zoología, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Concepción, Chile

    Oscar Inostroza-Michael & Cristián E. Hernández

  6. Centro de Investigación en Biodiversidad y Ambientes Sustentables (CIBAS), Facultad de Ciencias, Universidad Católica de la Santísima Concepción (UCSC), Concepción, Chile

    Reinaldo J. Rivera

  7. Universidad Católica de Santa María, Arequipa, Perú

    Cristián E. Hernández

  8. Centro i~mar, Universidad de Los Lagos, Puerto Montt, Chile

    Cristian B. Canales-Aguirre

  9. Núcleo Milenio INVASAL, Concepción, Chile

    Cristian B. Canales-Aguirre

Authors
  1. Jorge Avaria-Llautureo
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Contributions

J.A.-L. and C.B.C.-A. conceived the idea. J.A.-L. and C.V. designed the methodology and statistical models. J.A.-L. obtained the data, implemented the computer codes and analysed the data. C.E.H. provided computational support for data analysis. O.I.-M. obtained the data for maximum standard length. R.J.R. helped to obtain environmental data. J.A.-L. wrote the manuscript and made tables and figures. C.V., C.B.C.-A. and M.M.R. made substantial changes to the manuscript. All authors made comments on the final version of the manuscript.

Corresponding author

Correspondence to Jorge Avaria-Llautureo.

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The authors declare no competing interests.

Additional information

Peer review information Nature Climate Change thanks Sarah Friedman, Joseph Flannery Sutherland and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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

Extended data

Extended Data Fig. 1 Geographic distribution of Clupeiformes species used in this study.

Blue dots represent both the geographic occurrences obtained from Aquamaps and the random sample within IUCN polygons. We obtained 21,795 datapoints for 158 species. The paleo coordinates (red dots) for the fossils of Dorosoma (America) and Engraulidae (Europe) were estimated using the PALEOMAP model in the chronosphere R package, using the current coordinates of fossils (purple dots). The coordinates of extant species (blue dots) plus the two paleo coordinates (red dots) were used as input data to reconstruct ancestral locations across phylogenetic nodes.

Extended Data Fig. 2 Clupeiformes phylogenetic tree used in this study.

The phylogenetic tree was obtained from the Fish Tree of Life and represent the most updated topology and divergence times of the group. Note that branch colours represent the taxonomic arrangement of the group and are used for reference only. Fossils and type of migration are indicated. For the Geo model analyses we excluded Denticeps clupeoides (Methods). Nevertheless, we included D. cupleoides in all other analyses. Phylogeny species names, from top to bottom, are in the dataset available in the Dryad repository.

Extended Data Fig. 3 Posterior geographic distribution and posterior probability of habitat type for eight phylogenetic nodes.

We selected eight random nodes ranging from 111 to 33 Ma. a = 78 Mya; c = 56 Mya; e = 52 Mya; g = 41 Mya; i = 4 Mya; k = 38.8 Mya; m = 38.4 Mya; o = 36 Mya. The posterior coordinates were estimated with Geo model. b, d, f, h, j, j, I, n, p, the ancestral habitat type for these eight random nodes was estimated using phylogenetic models for discrete trait evolution.

Extended Data Fig. 4 Two continuous geographic routes for the lines of descent leading to Chirocentrus dorab and Engraulis australis.

The Geo model estimate the posterior probability of ancestral species locations (phylogenetic nodes) from georeferenced occurrences of individuals within extinct and extant species. Ancestral locations are estimated while allowing the speed of species movement to vary across phylogenetic branches. a, The circles and squares are the geographic centroid estimated from the posterior distribution of coordinates (at phylogenetic nodes in b) and the sample of coordinates from extant species. Note that the geographic centroids are used to obtain an example of the average route travelled for each species. However, we used 1,000 values of total distance and speed (using the full posterior distribution of estimated locations) for each species in all the analyses of this study. Note also that the map represents the actual location of continents – it is included for reference only.

Extended Data Fig. 5 The estimated location for Denticeps clupeiodes made their speed and distance of movement to be an outlier in regression analyses.

We removed D. clupeoides (red dot) from the Geo analyses because that species descends directly from the MRCA of Clupeiformes and its location is estimated near to the location of the MRCA. This means that species has dispersed a short distance in an exceptionally long time of 150 million years. This causes the speed (a) and distance (b) of movement for that species to be extremely low and far away from the rest of data when evaluating the correlates of speed and distance. We plot the mean speed and distance for all species.

Extended Data Fig. 6 Comparison between median temperatures inferred independently from the phylogenetic approach and the HadCM3L Earth-System-Model.

a, Comparison with sea temperature from the HadMC3L model. b, Comparison with air temperature from the HadMC3L model. We selected eight random nodes plus the MRCA of Clupeoidei for comparison.

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Avaria-Llautureo, J., Venditti, C., Rivadeneira, M.M. et al. Historical warming consistently decreased size, dispersal and speciation rate of fish. Nat. Clim. Chang. 11, 787–793 (2021). https://doi.org/10.1038/s41558-021-01123-5

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