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

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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Fig. 1: Sexual dimorphism in two species of cytheroid ostracods.
Fig. 2: Model-predicted extinction rate according to sexual size and shape dimorphism.

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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.

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Authors

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.

Corresponding author

Correspondence to Gene Hunt.

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The authors declare no competing interests.

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Extended data figures and tables

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’.

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.

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.

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

Supplementary information

Supplementary Table 1

Excel spreadsheet with model support information for all 576 models.

Reporting Summary

Supplementary Table 2

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

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

Supplementary Table 4

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

Supplementary Data

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

Supplementary Data

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

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Martins, M.J.F., Puckett, T.M., Lockwood, R. et al. High male sexual investment as a driver of extinction in fossil ostracods. Nature 556, 366–369 (2018). https://doi.org/10.1038/s41586-018-0020-7

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