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.

The genetic sex-determination system predicts adult sex ratios in tetrapods

Subjects

Abstract

The adult sex ratio (ASR) has critical effects on behaviour, ecology and population dynamics1,2, but the causes of variation in ASRs are unclear3,4. Here we assess whether the type of genetic sex determination influences the ASR using data from 344 species in 117 families of tetrapods. We show that taxa with female heterogamety have a significantly more male-biased ASR (proportion of males: 0.55 ± 0.01 (mean ± s.e.m.)) than taxa with male heterogamety (0.43 ± 0.01). The genetic sex-determination system explains 24% of interspecific variation in ASRs in amphibians and 36% in reptiles. We consider several genetic factors that could contribute to this pattern, including meiotic drive and sex-linked deleterious mutations, but further work is needed to quantify their effects. Regardless of the mechanism, the effects of the genetic sex-determination system on the adult sex ratio are likely to have profound effects on the demography and social behaviour of tetrapods.

This is a preview of subscription content

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Phylogenetic distribution of the ASR and genetic sex-determination systems across tetrapods.
Figure 2: Variation in the ASR as a function of the sex-determination system in amphibians, reptiles, mammals and birds, and across tetrapods (all four clades combined).

References

  1. 1

    Kokko, H. & Jennions, M. D. Parental investment, sexual selection and sex ratios. J. Evol. Biol. 21, 919–948 (2008)

    Article  PubMed  PubMed Central  Google Scholar 

  2. 2

    Le Galliard, J.-F., Fitze, P. S., Ferrière, R. & Clobert, J. Sex ratio bias, male aggression, and population collapse in lizards. Proc. Natl Acad. Sci. USA 102, 18231–18236 (2005)

    CAS  Article  ADS  Google Scholar 

  3. 3

    Liker, A., Freckleton, R. P. & Székely, T. The evolution of sex roles in birds is related to adult sex ratio. Nature Commun. 4, 1587 (2013)

    Article  ADS  CAS  Google Scholar 

  4. 4

    Székely, T., Weissing, F. J. & Komdeur, J. Adult sex ratio variation: implications for breeding system evolution. J. Evol. Biol. 27, 1500–1512 (2014)

    Article  PubMed  PubMed Central  Google Scholar 

  5. 5

    Donald, P. F. Adult sex ratios in wild bird populations. Ibis 149, 671–692 (2007)

    Article  Google Scholar 

  6. 6

    Trivers, R. L. in Sexual Selection and the Descent of Men (ed. Cambell, B. ) 136–179 (Aldine, 1972)

    Google Scholar 

  7. 7

    Cockburn, A., Scott, M. P. & Dickman, C. R. Sex ratio and intrasexual kin competition in mammals. Oecologia 66, 427–429 (1985)

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  8. 8

    Székely, T., Liker, A., Freckleton, R. P., Fichtel, C. & Kappeler, P. M. Sex-biased survival predicts adult sex ratio variation in wild birds. Proc. R. Soc. B 281, 20140342 (2014)

    Article  PubMed  PubMed Central  Google Scholar 

  9. 9

    Bessa-Gomes, C., Legendre, S. & Clobert, J. Allee effects, mating systems and the extinction risk in populations with two sexes. Ecol. Lett. 7, 802–812 (2004)

    Article  Google Scholar 

  10. 10

    Liker, A., Freckleton, R. P. & Székely, T. Divorce and infidelity are associated with skewed adult sex ratios in birds. Curr. Biol. 24, 880–884 (2014)

    CAS  Article  Google Scholar 

  11. 11

    Griskevicius, V. et al. The financial consequences of too many men: sex ratio effects on saving, borrowing, and spending. J. Pers. Soc. Psychol. 102, 69–80 (2012)

    Article  Google Scholar 

  12. 12

    Schacht, R., Rauch, K. L. & Borgerhoff Mulder, M. Too many men: the violence problem? Trends Ecol. Evol. 29, 214–222 (2014)

    Article  Google Scholar 

  13. 13

    Wilson, E. O. Sociobiology: The New Synthesis (Harvard Univ. Press, 1975)

    Google Scholar 

  14. 14

    Haldane, J. B. Sex-ratio and unisexual sterility in hybrid animals. J. Genet. 12, 101–109 (1922)

    Article  Google Scholar 

  15. 15

    Burt, A. & Trivers, R. Genes in Conflict: The Biology of Selfish Genetic Elements (Harvard Univ. Press, 2008)

    Google Scholar 

  16. 16

    Liker, A. & Székely, T. Mortality costs of sexual selection and parental care in natural populations of birds. Evolution 59, 890–897 (2005)

    Article  Google Scholar 

  17. 17

    Bachtrog, D. et al. Sex determination: why so many ways of doing it? PLoS Biol. 12, e1001899 (2014)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. 18

    Pagel, M. Inferring evolutionary processes from phylogenies. Zool. Scr. 26, 331–348 (1997)

    Article  Google Scholar 

  19. 19

    Pagel, M. Detecting correlated evolution on phylogenies: A general method for the comparative analysis of discrete characters. Proc. R. Soc. Lond. B 255, 37–45 (1994)

    Article  ADS  Google Scholar 

  20. 20

    Morrison, C. & Hero, J.-M. Geographic variation in life-history characteristics of amphibians: a review. J. Anim. Ecol. 72, 270–279 (2003)

    Article  Google Scholar 

  21. 21

    Adkins-Regan, E. & Reeve, H. K. Sexual dimorphism in body size and the origin of sex-determination systems. Am. Nat. 183, 519–536 (2014)

    Article  PubMed  PubMed Central  Google Scholar 

  22. 22

    Qi, Y., Yang, W., Lu, B. & Fu, J. Genetic evidence for male-biased dispersal in the Qinghai toad-headed agamid Phrynocephalus vlangalii and its potential link to individual social interactions. Ecol. Evol. 3, 1219–1230 (2013)

    Article  PubMed  PubMed Central  Google Scholar 

  23. 23

    Bachtrog, D. A dynamic view of sex chromosome evolution. Curr. Opin. Genet. Dev. 16, 578–585 (2006)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. 24

    Mank, J. E. Sex chromosome dosage compensation: definitely not for everyone. Trends Genet. 29, 677–683 (2013)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. 25

    Jaenike, J. Sex chromosome meiotic drive. Annu. Rev. Ecol. Syst. 32, 25–49 (2001)

    Article  Google Scholar 

  26. 26

    Werren, J. H. & Beukeboom, L. W. Sex determination, sex ratios, and genetic conflict. Annu. Rev. Ecol. Evol. Syst. 29, 233–261 (1998)

    Article  Google Scholar 

  27. 27

    Field, D. L., Pickup, M. & Barrett, S. C. H. Comparative analyses of sex-ratio variation in dioecious flowering plants. Evolution 67, 661–672 (2013)

    Article  PubMed  PubMed Central  Google Scholar 

  28. 28

    Hough, J., Immler, S., Barrett, S. C. H. & Otto, S. P. Evolutionarily stable sex ratios and mutation load. Evolution 67, 1915–1925 (2013)

    Article  PubMed  PubMed Central  Google Scholar 

  29. 29

    Roberts, R. B., Ser, J. R. & Kocher, T. D. Sexual conflict resolved by invasion of a novel sex determiner in Lake Malawi Cichlid fishes. Science 326, 998–1001 (2009)

    CAS  Article  ADS  PubMed  PubMed Central  Google Scholar 

  30. 30

    van Doorn, G. S. & Kirkpatrick, M. Transitions between male and female heterogamety caused by sex-antagonistic selection. Genetics 186, 629–645 (2010)

    Article  PubMed  PubMed Central  Google Scholar 

  31. 31

    Evans, B. J., Pyron, R. A. & Wiens, J. J. in Polyploidy and Genome Evolution (eds Soltis, P. S. & Soltis, D. E. ) 385–410 (Springer Berlin Heidelberg, 2012)

    Book  Google Scholar 

  32. 32

    Jongepier, E. Reptilian Adult Sex Ratios are Biased Towards the Homogametic Sex. Masters thesis, Univ. Groningen. (2011)

    Google Scholar 

  33. 33

    Arendt, J. D., Reznick, D. N. & López-Sepulcre, A. Replicated origin of female-biased adult sex ratio in introduced populations of the Trinidadian Guppy (Poecilia reticulata). Evolution 68, 2343–2356 (2014)

    PubMed  Google Scholar 

  34. 34

    The Tree of Sex Consortium Tree of Sex: A database of sexual systems. Sci. Data 1, 140015 (2014)

  35. 35

    Miura, I., Ohtani, H. & Ogata, M. Independent degeneration of W and Y sex chromosomes in frog Rana rugosa . Chromosome Res. 20, 47–55 (2012)

    CAS  Article  Google Scholar 

  36. 36

    Sarre, S. D., Ezaz, T. & Georges, A. Transitions between sex-determining systems in reptiles and amphibians. Annu. Rev. Genomics Hum. Genet. 12, 391–406 (2011)

    CAS  Article  Google Scholar 

  37. 37

    Pokorná, M. & Kratochvíl, L. Phylogeny of sex-determining mechanisms in squamate reptiles: are sex chromosomes an evolutionary trap? Zool. J. Linn. Soc. 156, 168–183 (2009)

    Article  Google Scholar 

  38. 38

    Freckleton, R. P., Harvey, P. H. & Pagel, M. Phylogenetic analysis and comparative data: a test and review of evidence. Am. Nat. 160, 712–726 (2002)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  39. 39

    Lislevand, T., Figuerola, J. & Székely, T. Avian body sizes in relation to fecundity, mating system, display behaviour and resource sharing. Ecology 88, 1605 (2007)

    Article  Google Scholar 

  40. 40

    Du, W., Robbins, T. R., Warner, D. A., Langkilde, T. & Shine, R. Latitudinal and seasonal variation in reproductive effort of the eastern fence lizard (Sceloporus undulatus). Integr. Zool. 9, 360–371 (2014)

    Article  PubMed  PubMed Central  Google Scholar 

  41. 41

    Iverson, J. B., Balgooyen, C. P., Byrd, K. K. & Lyddan, K. K. Latitudinal variation in egg and clutch size in turtles. Can. J. Zool. 71, 2448–2461 (1993)

    Article  Google Scholar 

  42. 42

    Jones, K. E. et al. PanTHERIA: a species-level database of life history, ecology, and geography of extant and recently extinct mammals. Ecology 90, 2648 (2009)

    Article  Google Scholar 

  43. 43

    Healy, K. et al. Ecology and mode of life explain lifespan variation in birds and mammals. Proc. R. Soc. Lond. B 281, 20140298 (2014)

    Article  Google Scholar 

  44. 44

    Lessells, C. M. & Boag, P. T. Unrepeatable repeatabilities? A common mistake. Auk 104, 116–121 (1987)

    Article  Google Scholar 

  45. 45

    Pyron, R. A. & Wiens, J. J. A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Mol. Phylogenet. Evol. 61, 543–583 (2011)

    Article  PubMed  PubMed Central  Google Scholar 

  46. 46

    Gardner, M. G., Hugall, A. F., Donnellan, S. C., Hutchinson, M. N. & Foster, R. Molecular systematics of social skinks: phylogeny and taxonomy of the Egernia group (Reptilia: Scincidae). Zool. J. Linn. Soc. 154, 781–794 (2008)

    Article  Google Scholar 

  47. 47

    Pyron, R. A., Burbrink, F. T. & Wiens, J. J. A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evol. Biol. 13, 93 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. 48

    Guillon, J.-M., Guery, L., Hulin, V. & Girondot, M. A large phylogeny of turtles (Testudines) using molecular data. Contrib. Zool. 81, 147–158 (2012)

    Article  Google Scholar 

  49. 49

    Jetz, W., Thomas, G. H., Joy, J. B., Hartmann, K. & Mooers, A. O. The global diversity of birds in space and time. Nature 491, 444–448 (2012)

    CAS  Article  ADS  PubMed  PubMed Central  Google Scholar 

  50. 50

    Meredith, R. W. et al. Impacts of the cretaceous terrestrial revolution and KPg extinction on mammal diversification. Science 334, 521–524 (2011)

    CAS  Article  ADS  PubMed  PubMed Central  Google Scholar 

  51. 51

    Fritz, S. A., Bininda-Emonds, O. R. P. & Purvis, A. Geographical variation in predictors of mammalian extinction risk: big is bad, but only in the tropics. Ecol. Lett. 12, 538–549 (2009)

    Article  Google Scholar 

  52. 52

    Chiari, Y., Cahais, V., Galtier, N. & Delsuc, F. Phylogenomic analyses support the position of turtles as the sister group of birds and crocodiles (Archosauria). BMC Biol. 10, 65 (2012)

    Article  PubMed  PubMed Central  Google Scholar 

  53. 53

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

    CAS  Article  ADS  PubMed  PubMed Central  Google Scholar 

  54. 54

    Maddison, W. P. & Maddison, D. R. Mesquite: a Modular System for Evolutionary Analysis http://mesquiteproject.org (2011)

    MATH  Google Scholar 

  55. 55

    Pagel, M. & Meade, A. Bayesian analysis of correlated evolution of discrete characters by reversible-jump Markov chain Monte Carlo. Am. Nat. 167, 808–825 (2006)

    Article  Google Scholar 

  56. 56

    R Development Core Team. R: A Language and Environment for Statistical Computing http://www.R-project.org (R Foundation for Statistical Computing, 2008)

  57. 57

    Orme, A. D. et al. caper: Comparative Analyses of Phylogenetics and Evolution in R (v.0.5). https://cran.r-project.org/web/packages/caper/index.html (2013)

    Google Scholar 

Download references

Acknowledgements

M. Pennell and G. Imreh helped construct the phylogeny figure. We thank T. H. Clutton-Brock, S. P. Otto, D. Bachtrog and K. Reinhold for suggestions, and R. P. Freckleton for advice on analyses. We were supported by the European Union (TÁMOP-4.2.2.B-15/1/KONV-2015-0004), and by the US National Science Foundation (DEB-0819901 to M.K.). T.S. was supported by a Humboldt Award and MTA-DE ‘Lendület’ grant in projects that lead to the current work. A.L. was supported by the Hungarian Scientific Research Fund (OTKA K112838) and a Marie Curie Intra-European Fellowship.

Author information

Affiliations

Authors

Contributions

T.S. and A.L. conceived the study. T.S., A.L. and V.B. designed the analyses. I.P., V.B., P.F.D. and A.L. collected the reptile, amphibian, mammalian and bird data, respectively. I.P., V.B. and A.L. conducted the analyses. M.K. developed the population genetic models. All authors wrote the paper.

Corresponding author

Correspondence to András Liker.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Phylogenetically corrected mean and s.e.m. of ASR in clades with different sex-determination systems.

Parameter estimates for the mean and associated s.e.m. were calculated by PGLS models18 presented in Extended Data Table 2 (with branch lengths estimated by Nee’s method54).

Extended Data Table 1 Detailed analyses of the effect of sex-determination system on the ASR.
Extended Data Table 2 Phylogenetically controlled analyses of the relationship between ASR and genetic sex-determination system using different branch length assumptions.

Supplementary information

Supplementary Information

This file contains Supplementary Information Parts 1 and 2 and Supplementary References. (PDF 587 kb)

Supplementary Data

This file contains the full dataset and references used in the phylogenetic analyses. (XLSX 63 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Pipoly, I., Bókony, V., Kirkpatrick, M. et al. The genetic sex-determination system predicts adult sex ratios in tetrapods. Nature 527, 91–94 (2015). https://doi.org/10.1038/nature15380

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

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