Abstract Understanding the evolutionary mechanisms underlying the maintenance of individual differences in behavior and physiology is a fundamental goal in ecology and evolution. The pace‐of‐life syndrome hypothesis is often invoked to explain the maintenance of such within‐population variation. This hypothesis predicts that behavioral traits are part of a suite of correlated traits that collectively determine an individual's propensity to prioritize reproduction or survival. A key assumption of this hypothesis is that these traits are underpinned by genetic trade‐offs among life‐history traits: genetic variants that increase fertility, reproduction and growth might also reduce lifespan. We performed a systematic literature review and meta‐analysis to summarize the evidence for the existence of genetic trade‐offs between five key life‐history traits: survival, growth rate, body size, maturation rate, and fertility. Counter to our predictions, we found an overall positive genetic correlation between survival and other life‐history traits and no evidence for any genetic correlations between the non‐survival life‐history traits. This finding was generally consistent across pairs of life‐history traits, sexes, life stages, lab vs. field studies, and narrow‐ vs. broad‐sense correlation estimates. Our study highlights that genetic trade‐offs may not be as common, or at least not as easily quantifiable, in animals as often assumed.
more »
« less
The evolution of age-specific resistance to infectious disease
Innate, infection-preventing resistance often varies between host life stages. Juveniles are more resistant than adults in some species, whereas the opposite pattern is true in others. This variation cannot always be explained by prior exposure or physiological constraints and so it has been hypothesized that trade-offs with other life-history traits may be involved. However, little is known about how trade-offs between various life-history traits and resistance at different life stages affect the evolution of age-specific resistance. Here, we use a mathematical model to explore how trade-offs with natural mortality, reproduction and maturation combine to affect the evolution of resistance at different life stages. Our results show that certain combinations of trade-offs have substantial effects on whether adults or juveniles are more resistant, with trade-offs between juvenile resistance and adult reproduction inherently more costly than trade-offs involving maturation or mortality (all else being equal), resulting in consistent evolution of lower resistance at the juvenile stage even when infection causes a lifelong fecundity reduction. Our model demonstrates how the differences between patterns of age-structured resistance seen in nature may be explained by variation in the trade-offs involved and our results suggest conditions under which trade-offs tend to select for lower resistance in juveniles than adults.
more »
« less
- Award ID(s):
- 1936334
- PAR ID:
- 10394245
- Date Published:
- Journal Name:
- Proceedings of the Royal Society B: Biological Sciences
- Volume:
- 290
- Issue:
- 1991
- ISSN:
- 0962-8452
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Juveniles are typically less resistant (more susceptible) to infectious disease than adults, and this difference in susceptibility can help fuel the spread of pathogens in age‐structured populations. However, evolutionary explanations for this variation in resistance across age remain to be tested.One hypothesis is that natural selection has optimized resistance to peak at ages where disease exposure is greatest. A central assumption of this hypothesis is that hosts have the capacity to evolve resistance independently at different ages. This would mean that host populations have (a) standing genetic variation in resistance at both juvenile and adult stages, and (b) that this variation is not strongly correlated between age classes so that selection acting at one age does not produce a correlated response at the other age.Here we evaluated the capacity of three wild plant species (Silene latifolia,S. vulgarisandDianthus pavonius) to evolve resistance to their anther‐smut pathogens (Microbotryumfungi), independently at different ages. The pathogen is pollinator transmitted, and thus exposure risk is considered to be highest at the adult flowering stage.Within each species we grew families to different ages, inoculated individuals with anther smut, and evaluated the effects of age, family and their interaction on infection.In two of the plant species,S. latifoliaandD. pavonius, resistance to smut at the juvenile stage was not correlated with resistance to smut at the adult stage. In all three species, we show there are significant age × family interaction effects, indicating that age specificity of resistance varies among the plant families.Synthesis. These results indicate that different mechanisms likely underlie resistance at juvenile and adult stages and support the hypothesis that resistance can evolve independently in response to differing selection pressures as hosts age. Taken together our results provide new insight into the structure of genetic variation in age‐dependent resistance in three well‐studied wild host–pathogen systems.more » « less
-
The insulin and insulin-like signalling (IIS) network plays an important role in mediating several life-history traits, including growth, reproduction and senescence. Although insulin-like growth factors (IGFs) 1 and 2 are both key hormones in the vertebrate IIS network, research on IGF2 in juveniles and adults has been largely neglected because early biomedical research on rodents found negligible IGF2 postnatal expression. Here, we challenge this assumption and ask to what degree IGF2 is expressed during postnatal life across amniotes by quantifying the relative gene expression of IGF1 and IGF2 using publicly available RNAseq data for 82 amniote species and quantitative polymerase chain reaction on liver cDNA at embryonic, juvenile and adult stages for two lizard, bird and mouse species. We found that (i) IGF2 is expressed postnatally across amniote species and life stages—often at a higher relative expression than IGF1 , contradicting rodent models; (ii) the lack of rodent postnatal IGF2 expression is due to phylogenetic placement, not inbreeding or artificial selection; and (iii) adult IGF2 expression is sex-biased in some species. Our results demonstrate that IGF2 expression is typical for amniotes throughout life, suggesting that a comprehensive understanding of the mechanisms mediating variation in life-history traits will require studies that measure both IGFs.more » « less
-
Predation is a major source of mortality in the early life stages of fishes and a driving force in shaping fish populations. Theoretical, modeling, and laboratory studies have generated hypotheses that larval fish size, age, growth rate, and development rate affect their susceptibility to predation. Empirical data on predator selection in the wild are challenging to obtain, and most selective mortality studies must repeatedly sample populations of survivors to indirectly examine survivorship. While valuable on a population scale, these approaches can obscure selection by particular predators. In May 2018, along the coast of Washington, USA, we simultaneously collected juvenile quillback rockfish Sebastes maliger from both the environment and the stomachs of juvenile coho salmon Oncorhynchus kisutch . We used otolith microstructure analysis to examine whether juvenile coho salmon were age-, size-, and/or growth-selective predators of juvenile quillback rockfish. Our results indicate that juvenile rockfish consumed by salmon were significantly smaller, slower growing at capture, and younger than surviving (unconsumed) juvenile rockfish, providing direct evidence that juvenile coho salmon are selective predators on juvenile quillback rockfish. These differences in early life history traits between consumed and surviving rockfish are related to timing of parturition and the environmental conditions larval rockfish experienced, suggesting that maternal effects may substantially influence survival at this stage. Our results demonstrate that variability in timing of parturition and sea surface temperature leads to tradeoffs in early life history traits between growth in the larval stage and survival when encountering predators in the pelagic juvenile stage.more » « less
-
null (Ed.)ABSTRACT Metabolism is thought to mediate the connection between environmental selection pressures and a broad array of life history tradeoffs, but tests are needed. High juvenile predation correlates with fast growth, which may be achieved via fast juvenile metabolism. Fast offspring metabolism and growth can create physiological costs later in life that should be minimized in species with low adult mortality. Yet, relationships between juvenile metabolism and mortality at offspring versus adult stages are unexplored. We found that post-natal metabolism was positively correlated with adult mortality but not nest predation rates among 43 songbird species on three continents. Nest predation, but not adult mortality, explained additional variation in growth rates beyond metabolism. Our results suggest that metabolism may not be the mechanism underlying the relationships between growth and mortality at different life stages.more » « less
An official website of the United States government

