Letter | Published:

High male sexual investment as a driver of extinction in fossil ostracods

Naturevolume 556pages366369 (2018) | Download Citation

Abstract

Sexual selection favours traits that confer advantages in the competition for mates. In many cases, such traits are costly to produce and maintain, because the costs help to enforce the honesty of these signals and cues1. Some evolutionary models predict that sexual selection also produces costs at the population level, which could limit the ability of populations to adapt to changing conditions and thus increase the risk of extinction2,3,4. Other models, however, suggest that sexual selection should increase rates of adaptation and enhance the removal of deleterious mutations, thus protecting populations against extinction3, 5, 6. Resolving the conflict between these models is not only important for explaining the history of biodiversity, but also relevant to understanding the mechanisms of the current biodiversity crisis. Previous attempts to test the conflicting predictions produced by these models have been limited to extant species and have thus relied on indirect proxies for species extinction. Here we use the informative fossil record of cytheroid ostracods—small, bivalved crustaceans with sexually dimorphic carapaces—to test how sexual selection relates to actual species extinction. We show that species with more pronounced sexual dimorphism, indicating the highest levels of male investment in reproduction, had estimated extinction rates that were ten times higher than those of the species with the lowest investment. These results indicate that sexual selection can be a substantial risk factor for extinction.

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References

  1. 1.

    Höglund, J. & Sheldon, B. C. The cost of reproduction and sexual selection. Oikos 83, 478–483 (1998).

  2. 2.

    Lande, R. Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 34, 292–305 (1980).

  3. 3.

    Kokko, H. & Brooks, R. Sexy to die for? Sexual selection and the risk of extinction. Ann. Zool. Fenn. 40, 207–219 (2003).

  4. 4.

    Tanaka, Y. Sexual selection enhances population extinction in a changing environment. J. Theor. Biol. 180, 197–206 (1996).

  5. 5.

    Lumley, A. J. et al. Sexual selection protects against extinction. Nature 522, 470–473 (2015).

  6. 6.

    Lorch, P. D., Proulx, S., Rowe, L. & Day, T. Condition-dependent sexual selection can accelerate adaptation. Evol. Ecol. Res. 5, 867–881 (2003).

  7. 7.

    Darwin, C. The Descent of Man, and Selection in Relation to Sex. (John Murray, London, 1871).

  8. 8.

    Andersson, M. Sexual Selection. (Princeton Univ. Press, Princeton, 1994).

  9. 9.

    Martínez-Ruiz, C. & Knell, R. J. Sexual selection can both increase and decrease extinction probability: reconciling demographic and evolutionary factors. J. Anim. Ecol. 86, 117–127 (2017).

  10. 10.

    Jacomb, F., Marsh, J. & Holman, L. Sexual selection expedites the evolution of pesticide resistance. Evolution 70, 2746–2751 (2016).

  11. 11.

    Reding, L. P., Swaddle, J. P. & Murphy, H. A. Sexual selection hinders adaptation in experimental populations of yeast. Biol. Lett. 9, 20121202 (2013).

  12. 12.

    Doherty, P. F. Jr et al. Sexual selection affects local extinction and turnover in bird communities. Proc. Natl Acad. Sci. USA 100, 5858–5862 (2003).

  13. 13.

    Bro-Jørgensen, J. Will their armaments be their downfall? Large horn size increases extinction risk in bovids. Anim. Conserv. 17, 80–87 (2014).

  14. 14.

    Sorci, G., Møller, A. P. & Clobert, J. Plumage dichromatism of birds predicts introduction success in New Zealand. J. Anim. Ecol. 67, 263–269 (1998).

  15. 15.

    McLain, D. K., Moulton, M. P. & Sanderson, J. G. Sexual selection and extinction: the fate of plumage-dimorphic and plumage-monomorphic birds introduced onto islands. Evol. Ecol. Res. 1, 549–565 (1999).

  16. 16.

    Morrow, E. H. & Fricke, C. Sexual selection and the risk of extinction in mammals. Proc. R. Soc. B 271, 2395–2401 (2004).

  17. 17.

    Prinzing, A., Brändle, M., Pfeifer, R. & Brandl, R. Does sexual selection influence population trends in European birds? Evol. Ecol. Res. 4, 49–60 (2002).

  18. 18.

    Thomas, G. H., Lanctot, R. B. & Székely, T. Can intrinsic factors explain population declines in North American breeding shorebirds? A comparative analysis. Anim. Conserv. 9, 252–258 (2006).

  19. 19.

    McLain, D. K., Moulton, M. P. & Redfearn, T. P. Sexual selection and the risk of extinction of introduced birds on oceanic islands. Oikos 74, 27–34 (1995).

  20. 20.

    Payne, J. L. et al. Extinction intensity, selectivity and their combined macroevolutionary influence in the fossil record. Biol. Lett. 12, 20160202 (2016).

  21. 21.

    Orzechowski, E. A. et al. Marine extinction risk shaped by trait–environment interactions over 500 million years. Glob. Change Biol. 21, 3595–3607 (2015).

  22. 22.

    Knell, R. J., Naish, D., Tomkins, J. L. & Hone, D. W. E. Sexual selection in prehistoric animals: detection and implications. Trends Ecol. Evol. 28, 38–47 (2013).

  23. 23.

    Cohen, A. C. & Morin, J. G. Patterns of reproduction in ostracodes: a review. J. Crustac. Biol. 10, 184–212 (1990).

  24. 24.

    Martins, M. J. F., Hunt, G., Lockwood, R., Swaddle, J. P. & Horne, D. J. Correlation between investment in sexual traits and valve sexual dimorphism in Cyprideis species (Ostracoda). PLoS ONE 12, e0177791 (2017).

  25. 25.

    Kamiya, T. Heterochronic dimorphism of Loxoconcha uranouchiensis (Ostracoda) and its implications for speciation. Paleobiology 18, 221–236 (1992).

  26. 26.

    Hunt, G. et al. Sexual dimorphism and sexual selection in cytheroidean ostracodes from the Late Cretaceous of the U.S. coastal plain. Paleobiology 43, 620–641 (2017).

  27. 27.

    Puckett, T. M. Santonian–Maastrichtian planktonic foraminiferal and ostracode biostratigraphy of the northern Gulf Coastal Plain, USA. Stratigraphy 2, 117–146 (2005).

  28. 28.

    Liow, L. H. & Nichols, J. D. in Quantitative Methods in Paleobiology The Paleontological Society Papers Vol. 16 (eds Alroy, J. & Hunt, G.) 81–94 (The Paleontological Society, New Haven, 2010).

  29. 29.

    Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference. 2nd edn, (Springer, New York, 2010).

  30. 30.

    Servedio, M. R. & Boughman, J. W. The role of sexual selection in local adaptation and speciation. Annu. Rev. Ecol. Evol. Syst. 48, 85–109 (2017).

  31. 31.

    Horne, D. J., Danielopol, D. L. & Martens, K. in Sex and Parthenogenesis. Evolutionary Ecology of Reproductive Modes in Non-marine Ostracods (ed. Martens, K.) 157–195 (Backhuys Publishers, Leiden, 1998).

  32. 32.

    Lüpold, S. et al. How sexual selection can drive the evolution of costly sperm ornamentation. Nature 533, 535–538 (2016).

  33. 33.

    Chapman, T., Liddle, L. F., Kalb, J. M., Wolfner, M. F. & Partridge, L. Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature 373, 241–244 (1995).

  34. 34.

    Stanley, S. M. An analysis of the history of marine animal diversity. Paleobiology 33, 1–55 (2007).

  35. 35.

    Holland, S. M. The stratigraphic distribution of fossils. Paleobiology 21, 92–109 (1995).

  36. 36.

    Payne, J. L., Bush, A. M., Heim, N. A., Knope, M. L. & McCauley, D. J. Ecological selectivity of the emerging mass extinction in the oceans. Science 353, 1284–1286 (2016).

  37. 37.

    Larina, E. et al. Upper Maastrichtian ammonite biostratigraphy of the Gulf Coastal Plain (Mississippi Embayment, southern USA). Cretac. Res. 60, 128–151 (2016).

  38. 38.

    White, G. C. & Burnham, K. P. Program MARK: survival estimation from populations of marked animals. Bird Study 46, S120–S139 (1999).

  39. 39.

    Laake, J. L. RMark: An R Interface for Analysis of Capture-Recapture Data with MARK. AFSC Processed Report No. 2013-01 (Alaska Fisheries Science Center, 2013).

  40. 40.

    Liow, L. H. & Finarelli, J. A. A dynamic global equilibrium in carnivoran diversification over 20 million years. Proc. R. Soc. B 281, 20132312 (2014).

  41. 41.

    Foote, M. et al. Rise and fall of species occupancy in Cenozoic fossil mollusks. Science 318, 1131–1134 (2007).

  42. 42.

    Raup, D. M. Mathematical models of cladogenesis. Paleobiology 11, 42–52 (1985).

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Acknowledgements

We thank L. Smith (LSU) and C. Sanford (NMNH) for help with access to museum specimens and C. Hall, C. Sweeney, J. Shaw, and J. Stedman for assistance in data collection. This research was supported by NSF-EAR 1424906 and the National Museum of Natural History, Smithsonian Institution.

Reviewer information

Nature thanks M. Gage, R. Knell and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Author information

Author notes

  1. These authors contributed equally: Maria João Fernandes Martins, Gene Hunt.

Affiliations

  1. Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, DC, USA

    • Maria João Fernandes Martins
    •  & Gene Hunt
  2. Department of Geography and Geology, The University of Southern Mississippi, Hattiesburg, MS, USA

    • T. Markham Puckett
  3. Department of Geology, The College of William and Mary, Williamsburg, VA, USA

    • Rowan Lockwood
  4. Department of Biology, The College of William and Mary, Williamsburg, VA, USA

    • John P. Swaddle

Authors

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  2. Search for T. Markham Puckett in:

  3. Search for Rowan Lockwood in:

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Contributions

G.H. and M.J.F.M. collected the sexual dimorphism data and performed the analyses; T.M.P. collected the stratigraphic data and helped with the collection of dimorphism data. R.L., J.P.S. and G.H. designed the project and M.J.F.M. and G.H. primarily wrote the paper.

Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to Gene Hunt.

Extended data figures and tables

  1. Extended Data Fig. 1 Stratigraphic section showing the occurrence of 93 species over time.

    a, Location map of Tennessee, Mississippi and Alabama. The locations of samples that were collected from the focal composite reference section in Mississippi (MSCRS, blue circles) and the composite section in Alabama, which were treated as a replicate (ALCRS, red triangles), are shown along with the additional samples in the database that were used to compute occupancy (crosses). b, Stratigraphic occurrences for the MSCRS are shown. Each grey circle represents the occurrence of a species in a sample, with each species labelled according to four-letter abbreviations given in Supplementary Table 4. The map was made using the R package ‘maps’.

  2. Extended Data Fig. 2 Estimated model coefficients relating sexual size and shape dimorphism to extinction.

    a, Sexual size dimorphism (DMsize). b, Shape dimorphism (DMshape). The best 40 models are shown, sorted in order of decreasing support. The model-averaged coefficients are shown on the far right as larger circles. These estimates integrate over all models, weighted by their support, appropriately accounting for uncertainty in model selection. Error bars are 95% confidence intervals generated by MARK software.

  3. Extended Data Fig. 3 Stratigraphic occurrences of species plotted with respect to shape dimorphism.

    Top, species in the family Trachyleberididae; bottom, all other species. Species are sorted left to right based on shape dimorphism, with more extreme dimorphism plotted towards the right and in warmer colours. Symbol size is proportional to occupancy (larger indicates more broadly distributed). In the Trachyleberididae, there is a clear visual indication that more strongly dimorphic species have shorter stratigraphic durations.

  4. Extended Data Table 1 Best supported models for extinction and speciation using occurrence data from a replicate reference section in central Alabama

Supplementary information

  1. Supplementary Table 1

    Excel spreadsheet with model support information for all 576 models.

  2. Reporting Summary

  3. Supplementary Table 2

    Species attributes used in the analysis: dimorphism, shape dimorphism, occupancy, and family membership. Used by the CMR script.

  4. Supplementary Table 3

    Sample attributes used in the analysis: sample abundance (total number of ostracodes), formation/member name, minimum and maximum sample age (in Ma). Used by the CMR script

  5. Supplementary Table 4

    List of species analyzed, including their assignment to taxonomic family and the four-letter code used in Extended Data Figure 1

  6. Supplementary Data

    This file contains an R script that runs the CMR analysis presented in Table 1

  7. Supplementary Data

    This file contains a MARK input file format with species occurrences by sample. Used by the CMR script

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DOI

https://doi.org/10.1038/s41586-018-0020-7

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