The environment shapes the evolution of secondary sexual traits by determining how their costs and benefits vary across the landscape. Given the thermal properties of dark coloration generally, temperature should crucially influence the costs, benefits and geographic diversification of many secondary sexual colour patterns. We tested this hypothesis using sexually selected wing coloration in a dragonfly. We find that greater wing coloration heats males – the magnitude of which improves flight performance under cool conditions but dramatically reduces it under warm conditions. In a colder region of the species’ range, behavioural observations of a wild population show that these thermal effects translate into greater territorial acquisition on thermally variable days. Finally, geo‐referenced photographs taken by citizen scientists reveal that this sexually selected wing coloration is dramatically reduced in the hottest portions of the species’ range. Collectively, our results underscore temperature's capacity to promote and constrain the evolution of sexual coloration.
While deploying immune defences early in ontogeny can trade-off with the production and maintenance of other important traits across the entire life cycle, it remains largely unexplored how features of the environment shape the magnitude or presence of these lifetime costs. Greater predation risk during the juvenile stage may particularly influence such costs by (1) magnifying the survival costs that arise from any handicap of juvenile avoidance traits and/or (2) intensifying allocation trade-offs with important adult traits. Here, we tested for predator-dependent costs of immune deployment within and across life stages using the dragonfly, Pachydiplax longipennis. We first examined how larval immune deployment affected two traits associated with larval vulnerability to predators: escape distance and foraging under predation risk. Larvae that were induced to mount an immune response had shorter escape distances but lower foraging activity in the presence of predator cues. We also induced immune responses in larvae and reared them through emergence in mesocosms that differed in the presence of large predatory dragonfly larvae (Aeshnidae spp.). Immune-challenged larvae had later emergence overall and lower survival in pools with predators. Immune-challenged males were also smaller at emergence and developed less sexually selected melanin wing coloration, but these effects were independent of predator treatment. Overall, these results highlight how mounting an immune defence early in ontogeny can have substantial ecological and physiological costs that manifest both within and across life stages.
Bacterial genomes encode various multidrug efflux pumps (MDR) whose specific conditions for fitness advantage are unknown. We show that the efflux pump MdtEF-TolC, in Escherichia coli , confers a fitness advantage during exposure to extreme acid (pH 2). Our flow cytometry method revealed pH-dependent fitness tradeoffs between bile acids (a major pump substrate) and salicylic acid, a membrane-permeant aromatic acid that induces a drug-resistance regulon but depletes proton motive force (PMF). The PMF drives MdtEF-TolC and related pumps such as AcrAB-TolC. Deletion of mdtE (with loss of pump MdtEF-TolC) increased the strain’s relative fitness during growth with or without salicylate or bile acids. However, when the growth cycle included a 2-h incubation at pH 2 (below the pH growth range), MdtEF-TolC conferred a fitness advantage. The fitness advantage required bile salts but was decreased by the presence of salicylate, whose uptake is amplified by acid. For comparison, AcrAB-TolC, the primary efflux pump for bile acids, conferred a PMF-dependent fitness advantage with or without acid exposure in the growth cycle. A different MDR pump, EmrAB-TolC, confered no selective benefit during growth in the presence of bile acids. Without bile acids, all three MDR pumps incurred a large fitness cost with salicylate when exposed at pH 2. These results are consistent with the increased uptake of salicylate at low pH. Overall, we showed that MdtEF-TolC is an MDR pump adapted for transient extreme-acid exposure; and that low pH amplifies the salicylate-dependent fitness cost for drug pumps. IMPORTANCE Antibiotics and other drugs that reach the gut must pass through stomach acid. Yet little is known of how extreme acid modulates the effect of drugs on gut bacteria. We find that extreme-acid exposure leads to a fitness advantage for a multidrug pump that otherwise incurs a fitness cost. At the same time, extreme acid amplifies the effect of salicylate selection against multidrug pumps. Thus, organic acids and stomach acid could play important roles in regulating multidrug resistance in the gut microbiome. Our flow cytometry assay provides a way to measure the fitness effects of extreme-acid exposure to various membrane-soluble organic acids including plant-derived nutrients and pharmaceutical agents. Therapeutic acids might be devised to control the prevalence of multidrug pumps in environmental and host-associated habitats.
1. When the breeding environment fluctuates across generations, reproductive traits may evolve plasticity that optimises the balance between survival and mating success for the prevailing environment.2. For sexually selected colouration, this balance can depend on environmental temperatures. Accordingly, breeding colouration often co-varies with temperature through space and time. However, whether such traits exhibit plasticity in response to environmental temperatures is poorly understood.3. In the present study, a dragonfly (Pachydiplax longipennis) was reared under ambient or experimentally warmed conditions and tested for plasticity in its intrasexually selected wing colouration. Although wing colouration improves male territorial success, these advantages are smaller under warmer conditions than cooler conditions. It was therefore predicted that males reared under the ambient thermal conditions of the study site (Cleveland, Ohio) would develop more wing colouration than those reared under experimentally warmed conditions. 4. Contrary to this prediction, males reared in warm larval temperatures produced more wing colouration. Thus, although the secondary sexual colouration of this species displays some thermal plasticity, it does not appear to be adaptive relative to the known thermal variation of intrasexual selection in this population. 5. Given that the environment often determines the strength and direction of sexual selection, future studies should consider the potential for non-adaptive, and even maladaptive, developmental plasticity in the sexually selected traits of insects.
Abstract. Organisms with complex life cycles commonly exhibit adaptive plasticity in the timing of transitions between life stages. While the threat of predation is predicted to induce earlier transitions, empirical support has been equivocal. When predation risk affects both the propensity to transition to the next life stage and the ability to reach the energetic thresholds necessary to complete the transition, only those individuals in the best physiological condition may be able to accelerate development and emerge earlier. To test this hypothesis, we followed uniquely marked dragonfly larvae (Pachydiplax longipennis) through emergence in pools where we factorially manipulated the presence of a large heterospecific predator (Anax junius) and cannibalism risk via conspecific size variation. Consistent with our hypothesis, high-condition larvae were more likely to emerge in the presence of the heterospecific predator than in its absence, and low-condition larvae were more likely to emerge in its absence than in its presence. Moreover, high-condition larvae emerged earlier when cannibalism risk was high than when it was low. Predation risk therefore has condition-dependent effects on emergence. As predation risk frequently affects resource accumulation, similar mechanisms across taxa could commonly underlie the incongruence between empirical results and theoretical expectations for predator-induced life-history variation.
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