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Climate and maternal effects modify sex ratios in a weakly dimorphic marsupial

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Abstract

There is growing evidence that the sex ratios of wild vertebrate populations are determined by mechanisms that are directly influenced by environmental characteristics. The Trivers–Willard (TWH) and extrinsic modification (EMH) hypotheses postulate differing determinants of mammalian offspring sex ratios. TWH states that mothers allocate resources according to their current condition and sex-specific offspring costs. EMH states that environmental forces that affect maternal condition determine offspring sex ratios, independently of maternal tactics of sex-biased allocation. We statistically assessed support for each of these hypotheses using long-term life histories of the allied rock-wallaby, Petrogale assimilis; a continuously breeding, polygynous, weakly dimorphic marsupial. We showed that birth sex ratios were equal and independent of maternal and environmental conditions. However, secondary sex ratios were male-biased under good environmental conditions and for high quality mothers or mothers in good condition. Sex differences in offspring survival contributed to these biases: (1) environmental conditions strongly influenced survival to pouch emergence (in support of EMH) and (2) maternal quality affected survival to the end of maternal care (in support of TWH). Environmental effects on survival were more important than maternal factors over the entire period of maternal care and contributed most to male-biased sex ratios at pouch emergence. In contrast, maternal mass was the best predictor of sex ratios at the end of maternal care—the life history stage where offspring body mass differed between the sexes.

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Acknowledgements

We gratefully acknowledge the contributions of Peter Spencer, Alan Horsup, and Robyn Delaney, and many field volunteers to the collection of the long-term data used for this research. We thank J-M. Gaillard, M. Festa-Bianchet, and an anonymous reviewer for constructive comments. This work was funded by research grants to S. Delean from James Cook University and to H. Marsh from the Queensland Environmental Protection Agency.

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Authors and Affiliations

  1. School of Earth & Environmental Sciences, James Cook University, Townsville, Qld 4811, Australia

    Steven Delean & Helene Marsh

  2. The Environment Institute and School of Earth & Environmental Sciences, University of Adelaide, Adelaide, SA 5005, Australia

    Steven Delean

  3. Australian Institute of Marine Science, PMB 3, Townsville MC, Qld 4810, Australia

    Glenn De’ath

Authors
  1. Steven Delean
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  2. Glenn De’ath
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  3. Helene Marsh
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Corresponding author

Correspondence to Steven Delean.

Additional information

Communicated by A. Schulte-Hostedde

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Table S1

Estimated mean body size and body mass of adult male (n = 62) and female (n = 65) Petrogale assimilis (>3 years of age). Ninety-five percent confidence intervals of body measurements are given in parentheses. Percent sexual size dimorphism = 100 × (log e (male size/female size)). Mean body size and mass were estimated using linear mixed-effects models with sex as the fixed effect. Individual identity was the random effect in the models to account for repeated measurements on each individual. (PDF 52 kb)

Table S2

Rank-order correlations among the maternal and environmental explanatory variables measured at the (1) birth, (2) pouch emergence, and (3) end of weaning life history stages used to explain variation in the sex ratio and survival of Petrogale assimilis offspring at Black Rock. Significance values are given in parentheses and bolded where <0.05. SOI, Southern Oscillation Index. At each stage, population size was correlated with the 6-month mean SOI. Also, maternal mass and condition index were positively correlated; however, this was a threshold relationship; the heaviest mothers were consistently in good condition, yet there was no correlation between mass and condition for mothers weighing less than 3.8 kg. (PDF 69 kb)

Table S3

Table S3-A. Model selection results for sets of candidate models examining variation in the birth sex ratio of Petrogale assimilis offspring associated with TWH, EMH and joint TWH/EMH. df, degrees of freedom; ΔAICc, difference in AICc between model and minimum AICc model; w i , Akaike model weights within candidate sets;%DE, percent deviance explained; overall w i , Akaike model weights across all models. Environmental predictors: R, cumulative 6-month rainfall (log(mm)); and S, mean 6-month Southern Oscillation Index. Maternal predictors: C, body condition; and M, body mass (kg). Additional predictors: P, population size. Random effects: r(ID), mother identity; r(Y), sampling year (both random effects fitted in all models but only listed where the only term(s) in the model). Table S3-B. Model selection results for sets of candidate models examining variation in survival of P. assimilis offspring from birth to pouch emergence associated with TWH, EMH, and joint TWH/EMH. df, degrees of freedom; ΔAICc, difference in AICc between model and minimum AICc model; w i , Akaike model weights within candidate sets; %DE, percent deviance explained; overall w i , Akaike model weights across all models. Environmental predictors: R, cumulative 6-month rainfall (log(mm)); and S, mean 6-month Southern Oscillation Index. Maternal predictors: C, body condition; and M, body mass (kg). Additional predictors: sex, offspring sex; P, population size. Random effects: r(ID), mother identity (fitted in all models but only listed where the only term in the model). Table S3-C. Model selection results for sets of candidate models examining variation in the pouch emergence sex ratio of P. assimilis offspring associated with TWH, EMH, and joint TWH/EMH. df, degrees of freedom; ΔAICc, difference in AICc between model and minimum AICc model; w i , Akaike model weights within candidate sets; %DE, percent deviance explained; overall w i , Akaike model weights across all models. Environmental predictors: R, cumulative 6-month rainfall (log(mm)); and S, mean 6-month Southern Oscillation Index. Maternal predictors: C, body condition; and M, body mass (kg). Additional predictors: P, population size. Random effects: r(ID), mother identity; r(Y), sampling year (both random effects fitted in all models but only listed where the only term(s) in the model). Table S3-D. Model selection results for sets of candidate models examining variation in survival of P. assimilis offspring from pouch emergence to weaning associated with TWH, EMH, and joint TWH/EMH. df, degrees of freedom; ΔAICc, difference in AICc between model and minimum AICc model; w i , Akaike model weights within candidate sets; %DE, percent deviance explained; overall w i , Akaike model weights across all models. Environmental predictors: R, cumulative 6-month rainfall (log(mm)); and S, mean 6-month Southern Oscillation Index. Maternal predictors: C, body condition; and M, body mass (kg). Additional predictors: sex, offspring sex; P, population size. Random effects: r(ID), mother identity (fitted in all models but only listed where the only term in the model). Table S3-E. Model selection results for sets of candidate models examining variation in the weaning sex ratio (i.e., the end of maternal care) of P. assimilis offspring associated with TWH, EMH, and joint TWH/EMH. df, degrees of freedom; ΔAICc, difference in AICc between model and minimum AICc model; w i , Akaike model weights within candidate sets; %DE, percent deviance explained; overall w i , Akaike model weights across all models. Environmental predictors: R, cumulative 6-month rainfall (log(mm)); and S, mean 6-month Southern Oscillation Index. Maternal predictors: C, body condition; and M, body mass (kg). Additional predictors: P, population size. Random effects: r(ID), mother identity; r(Y), sampling year (both random effects fitted in all models but only listed where the only term(s) in the model). Table S3-F. Model selection results for sets of candidate models examining variation in the body mass at weaning (i.e., the end of maternal care) for P. assimilis offspring associated with TWH, EMH, and joint TWH/EMH. df, degrees of freedom; ΔAICc, difference in AICc between model and minimum AICc model; w i , Akaike model weights within candidate sets; %DE, percent deviance explained; overall w i , Akaike model weights across all models. Environmental predictors: R, cumulative 6-month rainfall (log(mm)); and S, mean 6-month Southern Oscillation Index. Maternal predictors: C, body condition; and M, body mass (kg). Additional predictors: sex, offspring sex; A, offspring age; P, population size. Random effects: r(ID), mother identity (fitted in all models but only listed where the only term in the model). (PDF 102 kb)

Table S4

Summary results describing maternal and environmental factors that influenced the sex ratio and survival at each life history stage between birth and weaning for Petrogale assimilis at Black Rock. Accordance with the Trivers–Willard hypothesis (TWH), that predicts offspring sex ratios vary depending on maternal allocation of resources according to sex-specific offspring costs, and/or the extrinsic modification hypothesis (EMH), that predicts environmental forces that affect maternal condition determine offspring sex ratios, are described. ∝ represents the proportion of the specified sex; ↑ represent increases in the specified variable; PEP, permanent pouch emergence; SOI, Southern Oscillation Index; \( \overline X \) sex ratios are probability of male offspring. (PDF 84 kb)

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Delean, S., De’ath, G. & Marsh, H. Climate and maternal effects modify sex ratios in a weakly dimorphic marsupial. Behav Ecol Sociobiol 64, 265–277 (2009). https://doi.org/10.1007/s00265-009-0844-0

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