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An age-dependent ovulatory strategy explains the evolution of dizygotic twinning in humans

Nature Ecology & Evolution volume 4, pages 987–992 (2020)Cite this article

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Abstract

Dizygotic twinning, the simultaneous birth of siblings when multiple ova are released, is an evolutionary paradox. Twin-bearing mothers often have elevated fitness, but despite twinning being heritable, twin births occur only at low frequencies in human populations. We resolve this paradox by showing that twinning and non-twinning are not competing strategies; instead, dizygotic twinning is the outcome of an adaptive conditional ovulatory strategy of switching from single to double ovulation with increasing age. This conditional strategy, when coupled with the well-known decline in fertility as women age, maximizes reproductive success and explains the increase and subsequent decrease in the twinning rate with maternal age that is observed across human populations. We show that the most successful ovulatory strategy would be to always double ovulate as an insurance against early fetal loss, but to never bear twins. This finding supports the hypothesis that twinning is a by-product of selection for double ovulation rather than selection for twinning.

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Fig. 1: Declining prenatal survival and increasing double ovulation rates explain age-dependent twinning rates.
Fig. 2: Average per capita numbers of offspring surviving to 15 years (95% confidence intervals, n = 10) from simulations of the reproductive lives of 1,000 women.
Fig. 3: Results of mathematical modelling of the reproductive characteristics of different ovulatory strategies.

Data availability

The data have been uploaded to Dyad and are available at https://doi.org/10.5061/dryad.h70rxwdfw.

Code availability

The computer code has been uploaded to Dyad and is available at https://doi.org/10.5061/dryad.h70rxwdfw. This code is supplied by the authors with the request that future users of the code are aware that it represents an ongoing research programme and that they contact the authors in a collaborative spirit.

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Acknowledgements

C. Lively, D. Dudle, L. Simmons, C. Smock and D. Hruschka provided comments on the manuscript drafts. We thank N. LeBas for detailed discussions of these ideas. J.L.T. was supported by a Future Fellowship (grant no. FT110100500) from the Australian Research Council. R.C.S. and W.N.H. were funded by DePauw University Faculty Development Grants.

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Authors and Affiliations

  1. Department of Biology, DePauw University, Greencastle, IN, USA

    Wade N. Hazel

  2. School of Biological Sciences, The University of Western Australia, Crawley, Western Australia, Australia

    Robert Black

  3. Department of Mathematics, DePauw University, Greencastle, IN, USA

    Richard C. Smock

  4. London School of Hygiene and Tropical Medicine, London, UK

    Rebecca Sear

  5. Centre for Evolutionary Biology, School of Biological Sciences, The University of Western Australia, Crawley, Western Australia, Australia

    Joseph L. Tomkins

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  1. Wade N. Hazel
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Contributions

J.L.T. proposed the study. W.N.H. and J.L.T. began developing the approaches. R.S. provided the demographic data and background on the biology of twinning. R.C.S. and W.N.H. finalized the mathematical model. J.L.T. and R.B. finalized the simulation model. W.N.H. wrote the first draft of the manuscript, and all authors contributed to the completed manuscript.

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Correspondence to Wade N. Hazel or Joseph L. Tomkins.

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Extended data

Extended Data Fig. 1 Double ovulation as a threshold trait.

a, Three conditional (age-dependent) ovulatory strategies that differ in age of switching from single (dashed line) to double ovulation (solid line). b, Threshold trait depiction of a cohort of population with normally distributed variation in age at switching (mean age at switching from single to double ovulation is 30 yrs., SD of 3 yrs.). At age 27, the threshold (vertical line positioned at age 27) divides the population into individuals that double ovulate (those with switching ages less than 27) and single ovulate (those with switching ages greater than 27). c, As age increases, the fraction of double ovulators increases as a cumulative normal function as the threshold in b shifts to the right, increasing the fraction of the distribution of switching ages that is less than the threshold.

Extended Data Fig. 2 Age-dependent probabilities of live birth, and prenatal death from early losses, spontaneous abortion, and late losses.

a-c, points from Supplementary Table 3; lines are best fitting curves from least squared regression. a, Early loss of pregnancy (variable r in Supplementary Table 1); b. Spontaneous abortion (variable s in Supplementary Table 1); c, Late loss of pregnancy (variable t in Supplementary Table 1); d, Live birth (line from average of results in Fig. 1f; variable u in Supplementary Table 1).

Extended Data Fig. 3 Age-dependent probability of twin live births in double ovulators.

Probability of twin live births was calculated using equation 1, assuming declining probability of live birth with increasing maternal age as depicted in Extended Data Fig. 2d.

Supplementary information

Supplementary Information

Supplementary Figs. 1–3, Tables 1–3, methods and discussion.

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Hazel, W.N., Black, R., Smock, R.C. et al. An age-dependent ovulatory strategy explains the evolution of dizygotic twinning in humans. Nat Ecol Evol 4, 987–992 (2020). https://doi.org/10.1038/s41559-020-1173-y

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