Effects of genetic vs. environmental quality on condition-dependent morphological and life history traits in a neriid fly.

Condition is assumed to reflect both genes and environment, enabling condition-dependent signals to reveal genetic quality. However, because the phenotypic effects of variation in genetic quality could be masked by environmental heterogeneity, the contribution of genetic quality to phenotypic variation in fitness-related traits and condition-dependent signals remains unclear. We compared effects of ecologically relevant manipulations of environmental quality (nutrient dilution in the larval diet) and genetic quality (one generation of inbreeding) on male and female morphology, life history and reproductive performance in the neriid fly Telostylinus angusticollis. We found that larval diet quality had strong, positive effects on male and female body size, male secondary sexual traits, and aspects of male and female reproductive performance. By contrast, inbreeding had weak effects on most traits, and no trait showed clear and consistent effects of both environmental and genetic quality. Indeed, inbreeding effects on body size and male competitive performance were of opposite sign in rich vs. poor larval diet treatment groups. Our results suggest that environmental quality strongly affects condition, but the effects of genetic quality are subtle and environment-dependent in this species. These findings raise questions about the genetic architecture of condition and the potential for condition-dependent traits to function as signals of genetic quality.

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.

Sexual competition and the evolution of condition-dependent ageing.

Increased individual resources (condition) can be correlated with either increased or decreased longevity. While variation in resource acquisition and allocation can account for some of this variation, the general conditions that select for either pattern remain unclear. Previous models suggest that nonlinearity of payoffs from investment in reproduction (e.g., male secondary sexual traits) can select for high-condition individuals that sacrifice longevity to increase reproductive opportunity. However, it remains unclear what mating systems or patterns of sexual competition might select for such life-history strategies. We used a model of condition-dependent investment to explore how expected payoffs from increased expression of secondary sexual traits affect optimal investment in lifespan. We find that nonlinearity of these payoffs results in a negative relationship between condition and lifespan under two general conditions: first, when there are accelerating marginal benefits from increasing investment; second, when individuals that invest minimally in secondary sexual trait expression can still achieve matings. In the second scenario, the negative relationship occurs due to selection on low-condition individuals to extend lifespan at the cost of secondary sexual trait expression. Our findings clarify the potential role of sexual selection in shaping patterns of condition-dependent ageing, and highlight the importance of considering the strategies of both low- and high-condition individuals when investigating patterns of condition-dependent ageing.

Ontogenetic timing as a condition-dependent life history trait: High-condition males develop quickly, peak early, and age fast.

Within-population variation in ageing remains poorly understood. In males, condition-dependent investment in secondary sexual traits may incur costs that limit ability to invest in somatic maintenance. Moreover, males often express morphological and behavioral secondary sexual traits simultaneously, but the relative effects on ageing of investment in these traits remain unclear. We investigated the condition dependence of male life history in the neriid fly Telostylinus angusticollis. Using a fully factorial design, we manipulated male early-life condition by varying nutrient content of the larval diet and, subsequently, manipulated opportunity for adult males to interact with rival males. We found that high-condition males developed more quickly and reached their reproductive peak earlier in life, but also experienced faster reproductive ageing and died sooner than low-condition males. By contrast, interactions with rival males reduced male lifespan but did not affect male reproductive ageing. High-condition in early life is therefore associated with rapid ageing in T. angusticollis males, even in the absence of damaging male-male interactions. Our results show that abundant resources during the juvenile phase are used to expedite growth and development and enhance early-life reproductive performance at the expense of late-life performance and survival, demonstrating a clear link between male condition and ageing.