Final Report Summary - PATSUCCESS (Physiological and genetic drivers of male paternity success)
Understanding the forces that create variation in individual fitness underpins our ability to predict population and evolutionary dynamics and is consequently central to population and evolutionary biology. This project aimed at providing new insights into the forces that drive and constrain variation in male paternity success, one key component of male fitness, using a long-term study system on wild song sparrows.
One main aim of the project was to quantify genetic and environmental drivers of male paternity success. We therefore estimated additive genetic variance and heritability in male paternity success, and additive genetic covariance between male paternity success and female polyandry, providing the first tests of key hypotheses explaining the evolution of multiple mating. We first showed that male within-pair paternity success and extra-pair reproductive success, which are major component of a male’s reproductive success and fitness, are genetically inherited and hence have some potential to evolve (Reid et al., 2014, Journal of Evolutionary Biology). We further showed the existence of a positive genetic correlation, and hence a genetic synergy, between these two components of male reproductive success (Reid et al., 2014, Journal of Evolutionary Biology). Further, we also quantified the genetic correlation between female liability for extra-pair reproduction and male liability for within-pair paternity success, and highlighted an important genetic link between both sexes’ reproductive strategies (Reid et al, 2014a, Evolution).
Another main aim of the project was to estimate the effect of inbreeding, the reproduction among genetically related individuals, on male paternity success and on key sperm performance traits, thereby linking inbreeding with physiology and fitness. We first conducted a prospective meta-analysis and review on the effect of inbreeding on male gametic (i.e. sperm and pollen) traits, which indicated an overall significant but low inbreeding depression in gametic traits (Losdat et al. 2014, Journal of Evolutionary Biology). Our review showed that existing data are insufficient to draw clear conclusions and opens a new area for future research by highlighting the previously overlooked relative importance of haploid vs. diploid genetic control of gamete phenotypes, and the lack of studies in nature.
We further empirically quantified the effect of inbreeding on sperm performance using three years of data, and on male paternity success using 20 years of data, both combined with a long-term genetic pedigree on a wild song sparrow population. We first demonstrated a strong effect of inbreeding depression in male extra-pair reproductive success but not in within-pair paternity success (Reid et al., 2014, Journal of Evolutionary Biology). Second, we showed the existence of substantial variance in sperm swimming velocity, motility, or longevity, the main metrics of sperm performance, but our results surprisingly indicated no effect of inbreeding on these sperm traits (Losdat et al. In preparation). These data provide new insight on the mechanism underpinning the effect of inbreeding on male reproductive success, which may not primarily stem from reduced sperm performance in inbred males, but rather from inbreeding depression in other fitness-related traits such as behavioural traits.
The core of the project was complemented by two side objectives. First, we aimed at decomposing variance in male extra-pair reproductive success to identify the origin of the substantial variance observed in this fitness trait. We derived a novel variance decomposition that allows estimations of subcomponents of male extra-pair reproductive success and further applied it to 20 years of data on wild song sparrows. We thereby provide a new decomposition tool that can be used in other study systems and also showed that most of the variation in male extra-pair reproductive success comes from the probability of post-mating paternity success, which is also genetically inherited (Losdat et al., in revision in Journal of Animal Ecology). Second, we measured physiological stress in 350 song sparrows to test the hypotheses that individual physiological stress shows non-zero heritability and inbreeding depression, and hence that life-history evolution could be mediated by physiological stress (Losdat et al., submitted to Functional Ecology). We reported low heritability and hence demonstrated low potential for evolution of heterophil to lymphocyte ratio in wild song sparrows. Our results also indicated the existence of environmental-dependent inbreeding depression (Losdat et al., submitted to Functional Ecology).
One main aim of the project was to quantify genetic and environmental drivers of male paternity success. We therefore estimated additive genetic variance and heritability in male paternity success, and additive genetic covariance between male paternity success and female polyandry, providing the first tests of key hypotheses explaining the evolution of multiple mating. We first showed that male within-pair paternity success and extra-pair reproductive success, which are major component of a male’s reproductive success and fitness, are genetically inherited and hence have some potential to evolve (Reid et al., 2014, Journal of Evolutionary Biology). We further showed the existence of a positive genetic correlation, and hence a genetic synergy, between these two components of male reproductive success (Reid et al., 2014, Journal of Evolutionary Biology). Further, we also quantified the genetic correlation between female liability for extra-pair reproduction and male liability for within-pair paternity success, and highlighted an important genetic link between both sexes’ reproductive strategies (Reid et al, 2014a, Evolution).
Another main aim of the project was to estimate the effect of inbreeding, the reproduction among genetically related individuals, on male paternity success and on key sperm performance traits, thereby linking inbreeding with physiology and fitness. We first conducted a prospective meta-analysis and review on the effect of inbreeding on male gametic (i.e. sperm and pollen) traits, which indicated an overall significant but low inbreeding depression in gametic traits (Losdat et al. 2014, Journal of Evolutionary Biology). Our review showed that existing data are insufficient to draw clear conclusions and opens a new area for future research by highlighting the previously overlooked relative importance of haploid vs. diploid genetic control of gamete phenotypes, and the lack of studies in nature.
We further empirically quantified the effect of inbreeding on sperm performance using three years of data, and on male paternity success using 20 years of data, both combined with a long-term genetic pedigree on a wild song sparrow population. We first demonstrated a strong effect of inbreeding depression in male extra-pair reproductive success but not in within-pair paternity success (Reid et al., 2014, Journal of Evolutionary Biology). Second, we showed the existence of substantial variance in sperm swimming velocity, motility, or longevity, the main metrics of sperm performance, but our results surprisingly indicated no effect of inbreeding on these sperm traits (Losdat et al. In preparation). These data provide new insight on the mechanism underpinning the effect of inbreeding on male reproductive success, which may not primarily stem from reduced sperm performance in inbred males, but rather from inbreeding depression in other fitness-related traits such as behavioural traits.
The core of the project was complemented by two side objectives. First, we aimed at decomposing variance in male extra-pair reproductive success to identify the origin of the substantial variance observed in this fitness trait. We derived a novel variance decomposition that allows estimations of subcomponents of male extra-pair reproductive success and further applied it to 20 years of data on wild song sparrows. We thereby provide a new decomposition tool that can be used in other study systems and also showed that most of the variation in male extra-pair reproductive success comes from the probability of post-mating paternity success, which is also genetically inherited (Losdat et al., in revision in Journal of Animal Ecology). Second, we measured physiological stress in 350 song sparrows to test the hypotheses that individual physiological stress shows non-zero heritability and inbreeding depression, and hence that life-history evolution could be mediated by physiological stress (Losdat et al., submitted to Functional Ecology). We reported low heritability and hence demonstrated low potential for evolution of heterophil to lymphocyte ratio in wild song sparrows. Our results also indicated the existence of environmental-dependent inbreeding depression (Losdat et al., submitted to Functional Ecology).