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

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.

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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.

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Authors

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.

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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.

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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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