Silver-spoon upbringing improves early-life fitness but promotes reproductive ageing in a wild bird

Early-life conditions can have long-lasting effects and organisms that experience a poor start in life are often expected to age at a faster rate. Alternatively, individuals raised in high-quality environments can overinvest in early-reproduction resulting in rapid ageing. Here we use a long-term experimental manipulation of early-life conditions in a natural population of collared flycatchers (Ficedula albicollis), to show that females raised in a low-competition environment (artificially reduced broods) have higher early-life reproduction but lower late-life reproduction than females raised in high-competition environment (artificially increased broods). Reproductive success of high-competition females peaked in late-life, when low-competition females were already in steep reproductive decline and suffered from a higher mortality rate. Our results demonstrate that ‘silver-spoon’ natal conditions increase female early-life performance at the cost of faster reproductive ageing and increased late-life mortality. These findings demonstrate experimentally that natal environment shapes individual variation in reproductive and actuarial ageing in nature

Parental breeding age effects on descendants' longevity interact over 2 generations in matrilines and patrilines

Individuals within populations vary enormously in mortality risk and longevity, but the causes of this variation remain poorly understood. A potentially important and phylogenetically widespread source of such variation is maternal age at breeding, which typically has negative effects on offspring longevity. Here, we show that paternal age can affect offspring longevity as strongly as maternal age does and that breeding age effects can interact over 2 generations in both matrilines and patrilines. We manipulated maternal and paternal ages at breeding over 2 generations in the neriid fly Telostylinus angusticollis. To determine whether breeding age effects can be modulated by the environment, we also manipulated larval diet and male competitive environment in the first generation. We found separate and interactive effects of parental and grand-parental ages at breeding on descendants' mortality rate and life span in both matrilines and patrilines. These breeding age effects were not modulated by grand-parental larval diet quality or competitive environment. Our findings suggest that variation in maternal and paternal ages at breeding could contribute substantially to intrapopulation variation in mortality and longevity

Condition-dependence in life history evolution

Ageing is the progressive physiological deterioration that appears with increasing age and eventually leads to a decline in survival and reproduction. This physiological process is omnipresent across the tree of life, but the expected trajectory can widely vary between and within species. Classic theories predict that the evolution of senescence is strongly influenced by the level of extrinsic mortality. Furthermore, variation in early-life developmental environments can shape individual condition and thus lead to alternative life-history strategies. The interplay between early-life environment and individual condition might therefore predict the trajectory of ageing and is of importance when studying life history evolution. In this thesis, I focus on condition dependent life-history strategies and how this can translate in differential ageing patterns. Moreover, I specifically investigate the influence of early-life environment on key life history traits (i.e. survival and reproduction) and how this might eventually carry-over to future generations via nongenetic inheritance. First, I used an experimental approach involving lab populations of the nematode Caenorhabditis remanei to show that males, but not females, pay the cost for the evolution of increased lifespan (Paper I). Second, I used an empirical dataset based on 25 years of observations, to investigate the long-term effects of early-life environment on reproduction and survival (Paper II). Reproductive success of low-condition females in natural populations of collared flycatchers (Ficedula albicollis) peaks later in life, when high-condition females are already in steep reproductive decline and suffer from high mortality rates. Third, I used the neriid fly Telostylinus angusticollis in an experimental environment, to test whether condition-dependent investment in secondary sexual traits affects the life-history strategies of males (Paper III). High-condition males developed and aged faster than low-condition males, but interaction with rival males did not affect male reproductive ageing. Finally, continuing the T. angusticollis experiment, I also found that parental diet interacts with parental sex and offspring sex, ultimately affecting offspring life-histories. Parental effects can thus play an important role in shaping between-individual variation in reproductive and actuarial senescence (Paper IV). Overall, in this thesis I have explored the interaction between environment, condition and ageing in both experimental and natural settings

Condition-dependence in life history evolution

Ageing is the progressive physiological deterioration that appears with increasing age and eventually leads to a decline in survival and reproduction. This physiological process is omnipresent across the tree of life, but the expected trajectory can widely vary between and within species. Classic theories predict that the evolution of senescence is strongly influenced by the level of extrinsic mortality. Furthermore, variation in early-life developmental environments can shape individual condition and thus lead to alternative life-history strategies. The interplay between early-life environment and individual condition might therefore predict the trajectory of ageing and is of importance when studying life history evolution. In this thesis, I focus on condition dependent life-history strategies and how this can translate in differential ageing patterns. Moreover, I specifically investigate the influence of early-life environment on key life history traits (i.e. survival and reproduction) and how this might eventually carry-over to future generations via nongenetic inheritance. First, I used an experimental approach involving lab populations of the nematode Caenorhabditis remanei to show that males, but not females, pay the cost for the evolution of increased lifespan (Paper I). Second, I used an empirical dataset based on 25 years of observations, to investigate the long-term effects of early-life environment on reproduction and survival (Paper II). Reproductive success of low-condition females in natural populations of collared flycatchers (Ficedula albicollis) peaks later in life, when high-condition females are already in steep reproductive decline and suffer from high mortality rates. Third, I used the neriid fly Telostylinus angusticollis in an experimental environment, to test whether condition-dependent investment in secondary sexual traits affects the life-history strategies of males (Paper III). High-condition males developed and aged faster than low-condition males, but interaction with rival males did not affect male reproductive ageing. Finally, continuing the T. angusticollis experiment, I also found that parental diet interacts with parental sex and offspring sex, ultimately affecting offspring life-histories. Parental effects can thus play an important role in shaping between-individual variation in reproductive and actuarial senescence (Paper IV). Overall, in this thesis I have explored the interaction between environment, condition and ageing in both experimental and natural settings

Digest : Life history evolution in Darwin's dream ponds

Can variation in sex‐specific parental investment lead to sexual dimorphism in immune response? Keller et al. (2018) measured immune cell parameters, expression of candidate genes and composition of buccal microbiota in mouthbrooding cichlid species from Lake Tanganyika that show either maternal or biparental care. They found that maternal mouthbrooding species have increased sexual dimorphism in immune parameters, while biparental mouthbrooders exhibit an upregulated adaptive immune response, suggesting resource allocation shifts between parental investment and the immune system

Data from: Evolution of male age-specific reproduction under differential risks and causes of death: males pay the cost of high female fitness

Classic theories of ageing evolution predict that increased extrinsic mortality due to an environmental hazard selects for increased early reproduction, rapid ageing and short intrinsic lifespan. Conversely, emerging theory maintains that when ageing increases susceptibility to an environmental hazard, increased mortality due to this hazard can select against ageing in physiological condition and prolong intrinsic lifespan. However, evolution of slow ageing under high-condition-dependent mortality is expected to result from reallocation of resources to different traits and such reallocation may be hampered by sex-specific trade-offs. Because same life-history trait values often have different fitness consequences in males and females, sexually antagonistic selection can preserve genetic variance for lifespan and ageing. We previously showed that increased condition-dependent mortality caused by heat shock leads to evolution of long-life, decelerated late-life mortality in both sexes and increased female fecundity in the nematode, Caenorhabditis remanei. Here, we used these cryopreserved lines to show that males evolving under heat shock suffered from reduced early-life and net reproduction, while mortality rate had no effect. Our results suggest that heat-shock resistance and associated long-life trade-off with male, but not female, reproduction and therefore sexually antagonistic selection contributes to maintenance of genetic variation for lifespan and fitness in this population

male rep aging data

male rep aging dat

Temperature-induced compensatory growth in C. elegans is regulated by thermosensitive TRP channel and increases reproductive fitness

Animals are often not growing at the maximum rate, but can compensate for a bad start of life by subsequently increasing growth rate. While this compensatory growth is widespread, its direct fitness consequences are seldom investigated and its genetic basis is unknown.We investigated the genetic regulation, as well as fitness and lifespan consequences of compensatory growth in response to temperature, using Caenorhabditis elegans knockout of the thermo-sensitive TRP ion channel TRPA-1, involved in temperature recognition. We exposed juvenile worms to cold, favourable (intermediate) or warm temperatures in order to delay or speed up development.Wild-type worms initially exposed to cold temperature experienced slower growth but after being switched to a more favourable temperature, they expressed compensatory growth and caught up in size. Those initially reared at warmer temperatures than favourable experienced slower growth and attained smaller adult size after being switched to the most favourable temperature.Compensatory growth also altered the reproductive schedule. While rate-sensitive individual fitness decreased by cold juvenile temperatures, as a direct effect of the substantial developmental delay, once worms returned to more favourable temperature, they shifted their reproductive schedule towards early reproduction. Therefore, when focusing on the post-treatment period, the reproductive rate increased even though lifetime reproductive success was unaffected. Surprisingly, compensatory growth did not reduce adult lifespan. In contrast to the findings for wild-type worms, juvenile temperature did not induce compensatory or slowed-down growth in the trpa-1 knockout mutants.We thus show that the trpa-1 is involved in the network regulating temperature-induced compensatory growth in C. elegans and that this compensatory growth can influence the reproductive rate