Sex allocation, terminal investment and the effects of environmental constraints on maternal investment in subtropical antechinus Daniela V. Parra Faundes Bachelor of Science, Master of Science A thesis submitted for the degree of Doctor of Philosophy at The University of Queensland in 2014 School of Biological Sciences Cover photo: Female subtropical antechinus named Olive, born in 2012, hand-reared by Daniela Parra-Faundes and released back to the wild on mid-January 2013. This picture was taken three weeks after she was released. Photo: Daniela Parra-Faundes ii Abstract This thesis addresses questions on sex allocation, life history strategies and costs of reproduction using experimental manipulations of litter sex ratios and field data on ecology and behaviour of the subtropical antechinus (Antechinus subtropicus). In chapter 2, I investigate two major adaptive hypotheses to explain sex ratio bias at birth: the Trivers-Willard Hypothesis (TWH) and the Local Resource Competition Hypothesis (LRCH). I show that sons are more costly to produce than daughters because they have fast growth rates and there are greater survival costs to mothers when they wean more sons. Mothers that naturally produced male-biased litters were slightly heavier than mothers that gave birth to female-biased litters. These results are consistent with the TWH, which states that mothers with more resources to invest benefit by producing high quality competitive sons that will reproduce. However, after increasing the natural bias of litter sex ratios, mothers were able to increase investment to meet demands of rearing more sons than they had naturally produced, without compromising offspring growth. These results are inconsistent with a key prediction of the TWH, that females give birth to the number of sons that they can afford to raise. Also inconsistent with the TWH, male- biased litters grew more quickly after the sex ratio manipulation and, were more likely to survive to weaning. The LRCH predicts that mothers in poor condition should reduce competition from the sex that competes the most, by allocating more to sons than to daughters, as females often remain in their natal home range after weaning. In support of the LRCH, large litter size was associated with slower growth rate in daughters, but not sons. These results differ from previous cross fostering manipulations to test sex allocation in mammals, which have unequivocally supported the TWH. In chapter 3 I examine changes in reproductive performance and survival with age in females. Senescence and terminal investment are two major models to understand effects of age on reproduction. Reproductive investment and success declines with age if senescence occurs, and investment in young increases near the end of life if terminal investment occurs, improving offspring performance at a cost to mothers. I show that older subtropical antechinuses females are not reproductively senescent. On the contrary, females had a greater investment ability and an overall improvement in reproductive performance with age. Older mothers increased investment in their second litters, and were able to produce high quality, large, fast growing offspring that were also more likely iii to survive that the offspring from younger females. However, this greater maternal reduced their own survival. These results provide support for the terminal investment hypothesis (Cockburn 1994, Fisher & Blomberg 2011). Consistent costs of reproduction and terminal investment have often been difficult to demonstrate in wild mammals. My results confirm that marsupials are excellent models to address questions in life history evolution. In chapter 4 I investigate how rainfall patterns in relation to the reproductive cycle affects demography. I find that reproductive success of subtropical antechinuses is extremely sensitive to changes in environmental conditions, and that both the timing and magnitude of drought are important and may cause severe declines in the whole population. I show that growth, survival and body condition of individuals of this species are driven by rainfall, especially during lactation and weaning. During this study, the pattern of rainfall varied caused by strong effects of La Niña during 2010 and 2011, that ended 14 years of drought. Rainfall peaks varied in relation to the different stages of the reproductive season (mating, pregnancy, lactation and weaning) of subtropical antechinuses at Springbrook National Park. Overall, low rainfall during lactation reduced maternal condition and investment abilities that were evident by their reduced body mass, offspring growth, weaning success and survival of both mothers and offspring. Younger mothers and male offspring were most affected. In contrast, high rainfall throughout lactation increased maternal investment abilities as they were able to produce high quality, large offspring that were more likely to survive and breed. These high quality offspring also showed a greater investment ability themselves, by producing large, fast growing offspring, suggesting that the resulting increase in quality persisted throughout their lives. Younger mothers were the most favoured by good environmental conditions during lactation as their survival was greatly increased. However, survival of offspring as independent juveniles relies heavily on the predictability and abundance of rainfall during summer at weaning time. Low rainfall at the time when juveniles start to fend for themselves drastically reduced their survival, even if there was high rainfall during lactation. I conclude that growth and survival are determined by fluctuating environmental conditions in this species, in addition to sex allocation and maternal investment which depend on resource availability. iv Declaration by author This thesis is composed of my original work, and contains no material previously published or written by another person except where due reference has been made in the text. I have clearly stated the contribution by others to jointly-authored works that I have included in my thesis. I have clearly stated the contribution of others to my thesis as a whole, including statistical assistance, survey design, data analysis, significant technical procedures, professional editorial advice, and any other original research work used or reported in my thesis. The content of my thesis is the result of work I have carried out since the commencement of my research higher degree candidature and does not include a substantial part of work that has been submitted to qualify for the award of any other degree or diploma in any university or other tertiary institution. I have clearly stated which parts of my thesis, if any, have been submitted to qualify for another award. I acknowledge that an electronic copy of my thesis must be lodged with the University Library and, subject to the General Award Rules of The University of Queensland, immediately made available for research and study in accordance with the Copyright Act 1968. I acknowledge that copyright of all material contained in my thesis resides with the copyright holder(s) of that material. Where appropriate I have obtained copyright permission from the copyright holder to reproduce material in this thesis. v Publications during candidature Book chapter: Parra-Faundes DV, Fisher DO. (in press). Maternal care strategies of marsupial and implications for animal welfare. In: Animal Welfare: mother and young. Elsevier B.V. (Appendix). Conference abstract: Parra-Faundes DV, Goldizen AW, Fisher DO. 2012. Sex allocation in the subtropical antechinus: effects of sex ratio manipulation on survival and growth of mothers and their young. 58th Scientific Meeting of the Australian Mammal Society, p. 39, Port Augusta, Australia. Publications included in this thesis Book chapter (Appendix). Parra-Faundes DV, Fisher DO. (in press). Maternal care strategies of marsupial and implications for animal welfare. In: Animal Welfare: mother and young. Elsevier B.V. Contributor Statement of contribution Daniela Parra Faundes (Candidate) Wrote the paper (70%) Diana Fisher Wrote and edited paper (30%) vi Contributions by others to the thesis Diana Fisher assisted in developing the ideas for this thesis and obtained research funds to support this project. Diana Fisher and Anne Goldizen contributed to discuss results and both helped editing the manuscripts. Simon Blomberg provided statistical advice to analyse data. The candidate performed all field work and data collection, performed the statistical analyses and wrote all the manuscripts. Chapters 2 to 4 were written as papers for publication in peer-reviewed scientific journals, but they have not been sent yet. All co- authors consented to the manuscripts being included in this thesis. Additional contributions can be found in more detail in the acknowledgements section. Chapter 1: General introduction. The candidate wrote the manuscript. Diana Fisher and Anne Goldizen commented and help editing the written drafts of the chapter. Chapter 2: An experimental test of the Trivers Willard and Local Resource Competition hypotheses using three generations of cross fostering in the subtropical antechinus. Daniela Parra-Faundes (candidate) contributed to the experimental design (70%), performed field work and data collection (100%), wrote the manuscript (100%), performed the statistical analyses (100%), edited the paper (20%). Anne Goldizen helped discussing and interpreting results and edited the manuscript (30%). Diana Fisher provide the funds