Paternal Condition Drives Progeny Sex-Ratio Bias in a Lizard That Lacks Parental Care

Abstract

Sex-allocation theory predicts that females in good condition should preferentially produce offspring of the sex that benefits the most from an increase in maternal investment. However, it is generally assumed that the condition of the sire has little effect on progeny sex ratio, particularly in species that lack parental care. We used a controlled breeding experiment and molecular paternity analyses to examine the effects of both maternal and paternal condition on progeny sex ratio and progeny fitness in the brown anole (Anolis sagrei), a polygynous lizard that lacks parental care. Contrary to the predictions of sex-allocation theory, we found no relationship between maternal condition and progeny sex ratio. By contrast, progeny sex ratio shifted dramatically from female-biased to male-biased as paternal condition increased. This pattern was driven entirely by an increase in the production of sons as paternal condition improved. Despite strong natural selection favoring large size and high condition in both sons and daughters, we found no evidence that progeny survival was related to paternal condition. Our results emphasize the importance of considering the paternal phenotype in studies of sex allocation and highlight the need for further research into the pathways that link paternal condition to progeny fitness. In their landmark paper on adaptive sex allocation, Trivers and Willard (1973) hypothesized that mothers in a good physiological condition should bias the sex ratio of their progeny in favor of the sex that provides the greatest relative fitness return for a given increase in maternal investment. This influential idea has sparked numerous theoretical extensions and empirical tests in what has become one of the most active research areas in evolutionary biology

Mothers adjust offspring sex to match the quality of the rearing environment

“…Nevertheless, there is growing evidence for the role of paternal effects in adaptive sex allocation (e.g. lizards [53,54]), and further studies in birds are required to rigorously test these possibilities.…”

“…Since males were also fed the same experimental diet as females (once they were paired to females), one possibility is that paternal condition may influence sex allocation [53]. For example, fathers in inferior condition may reduce provisioning and care to their offspring, potentially providing direct benefits to females for adaptive sex allocation.…”

The Diversity, Plasticity, and Evolution of Sperm Morphology in Anolis Lizards

“…In wild populations of brown anoles, I found a similar significant negative relationship between condition and midpiece length. In re-analysis of paternity results from a previous experiment (Cox et al 2011) where males were allowed to copulate ad libitum with a female, I found that males in high condition sired more offspring than males in low condition. In competitive matings between males in the experimental diet treatments where males were limited to a single copulation, there was no effect of condition on fertilization success.…”

“…The brown anole has high rates of multiple paternity , and has extended sperm storage (Chapter 4), making it likely that this species experiences high levels of sperm competition. Additionally, in laboratory breeding designs where two age-matched males were mated to a single female with no male-male competition, large males and males with higher body condition tend to produce more offspring and sons than daughters, suggesting a postcopulatory mechanism that creates these biases (Cox et al 2011; Chapter 4).…”

“…We tested for condition-dependent fertilization success using data from the fertilization trials described above, in which condition was experimentally altered via dietary manipulation, and by analyzing data from a previous study in which captive-bred males varied naturally in condition (Cox et al 2011). The design of this previous study was similar to that described above, with each female mated sequentially to two males, and each pair of males mated to two females, once as the first and once as the second male to mate.…”