As organisms age, the effectiveness of natural selection weakens, leading to age-related decline in fitness-related traits. The evolution of age-related changes associated with senescence is likely influenced by mutation accumulation (MA) and antagonistic pleiotropy (AP). MA predicts that age-related decline in fitness components is driven by age-specific sets of alleles, nonnegative genetic correlations within trait across age, and an increase in the coefficient of genetic variance. AP predicts that age-related decline in a trait is driven by alleles with positive effects on fitness in young individuals and negative effects in old individuals, and is expected to lead to negative genetic correlations within traits across age. We build on these predictions using an association mapping approach to investigate the change in additive effects of SNPs across age and among traits for multiple stress-response fitness-related traits, including cold stress with and without acclimation and starvation resistance. We found support for both MA and AP theories of aging in the age-related decline in stress tolerance. Our study demonstrates that the evolution of age-related decline in stress tolerance is driven by a combination of alleles that have age-specific additive effects, consistent with MA, as well as nonindependent and antagonistic genetic architectures characteristic of AP.
Understanding how thermal selection affects phenotypic distributions across different time scales will allow us to predict the effect of climate change on the fitness of ectotherms. We tested how seasonal temperature variation affects basal levels of cold tolerance and two types of phenotypic plasticity in Drosophila melanogaster. Developmental acclimation occurs as developmental stages of an organism are exposed to seasonal changes in temperature and its effect is irreversible, while reversible short-term acclimation occurs daily in response to diurnal changes in temperature. We collected wild flies from a temperate population across seasons and measured two cold tolerance metrics (chill-coma recovery and cold stress survival) and their responses to developmental and short-term acclimation. Chill-coma recovery responded to seasonal shifts in temperature, and phenotypic plasticity following both short-term and developmental acclimation improved cold tolerance. This improvement indicated that both types of plasticity are adaptive, and that plasticity can compensate for genetic variation in basal cold tolerance during warmer parts of the season when flies tend to be less cold tolerant. We also observed a significantly stronger trade-off between basal cold tolerance and short-term acclimation during warmer months. For the longer-term developmental acclimation, a trade-off persisted regardless of season. A relationship between the two types of plasticity may provide additional insight into why some measures of thermal tolerance are more sensitive to seasonal variation than others. K E Y W O R D Sacclimation, daily temperature, developmental plasticity, evolutionary constraint, seasonal temperature
A range of heavy metals are required for normal cell function and homeostasis. However, the anthropogenic release of metal compounds into soil and water sources presents a pervasive health threat. Copper is one of many heavy metals that negatively impacts diverse organisms at a global scale. Using a combination of quantitative trait locus (QTL) mapping and RNA sequencing in the Drosophila Synthetic Population Resource, we demonstrate that resistance to the toxic effects of ingested copper in D. melanogaster is genetically complex and influenced by allelic and expression variation at multiple loci. QTL mapping identified several QTL that account for a substantial fraction of heritability. Additionally, we find that copper resistance is impacted by variation in behavioral avoidance of copper and may be subject to life-stage specific regulation. Gene expression analysis further demonstrated that resistant and sensitive strains are characterized by unique expression patterns. Several of the candidate genes identified via QTL mapping and RNAseq have known copper-specific functions (e.g., Ccs, Sod3, CG11825), and others are involved in the regulation of other heavy metals (e.g., Catsup, whd). We validated several of these candidate genes with RNAi suggesting they contribute to variation in adult copper resistance. Our study illuminates the interconnected roles that allelic and expression variation, organism life stage, and behavior play in copper resistance, allowing a deeper understanding of the diverse mechanisms through which metal pollution can negatively impact organisms.
We report on the discovery of a remarkable defensive specialization in stonefishes that was identified during a phylogenetic study of scorpionfishes and their relatives. This newly described innovation, the lachrymal saber, involves modifications to the circumorbitals, maxilla, adductor mandibulae, and associated tendons. At its core, the lachrymal saber is an elongation of an anterior spine (or spines) on the ventral surface of the lachrymal that stonefishes are capable of rotating from the standard ventral position to a locked lateral position. The locking mechanism minimally includes a bony spur on the inner surface of the lachrymal and a ridged bony protuberance on the anterolateral end of the maxilla. A modified and highly subdivided adductor mandibulae appears to control the movement of the lachrymal saber by rotating the maxilla while it is engaged with the spur on the medial side of the lachrymal. This maxillary rotation results in a subsequent rotation of the lachrymal that we hypothesize reduces predation on stonefishes. This specialization was included in our phylogenetic analysis of scorpaenoid fishes. This study expands upon the previous higher-level taxonomic sampling reported in earlier evolutionary studies of scorpaenoid fishes and, unlike previous analyses, explicitly combines molecular and morphological data with an expanded taxonomic sampling to mitigate the conflict between these competing datasets. The resulting phylogeny based on a combination of 113 morphological and 5,280 molecular characters for 63 species is used to produce a revised taxonomy of flatheads, scorpionfishes, sea robins, and stonefishes. Our results do not support the monophyly of the traditional Scorpaeniformes, Scorpaenoidei, Scorpaenoidea, Platycephaloidea, Bembridae, Scorpaenidae, Sebastidae, Serranidae, Tetrarogidae, or Triglidae. Our monophyletic taxonomy recognizes nine monophyletic families: Bembridae, Congiopodidae, Hoplichthyidae, Neosebastidae, Platycephalidae, Plectrogeniidae, Scorpaenidae, Synanceiidae, and Triglidae. The taxonomic composition of the Congiopodidae, Hoplichthyidae, Neosebastidae, and Platycephalidae are unchanged. The Bembridae is expanded to include the recently described Parabembridae, while Bembradium is moved to the Plectrogeniidae. The Scorpaenidae is expanded to include the traditional Sebastidae and Setarchidae. The Triglidae is expanded to include the Peristediidae. Finally, a revised Synanceiidae, diagnosed by the lachrymal saber, is expanded to include the Apistidae, Aploactinidae, Eschmeyeridae, Gnathanacanthidae, Pataecidae, Perryenidae, and Tetrarogidae. Based on these results, we recommend treating all of these traditional scorpaenoid clades as families in an expanded Scorpaeniformes that includes a restricted Scorpaenoidei that includes all traditional scorpaenoid families except the Congiopodidae. The resulting phylogeny is then used to explore aspects of scorpaenoid evolution.
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