Organisms vary widely in size from microbes weighing 0.1 picograms to trees weighing thousands of megagrams, a 10 21-fold range similar to the difference in mass between an elephant and the Earth. Mass has a pervasive influence on biological processes but the effect is usually non-proportional; for example, a 10-fold increase in mass is typically accompanied by just a 4-to-7-fold increase in metabolic rate. Understanding the cause of allometric scaling has been a long-standing problem in biology. Here, we examine the evolution of metabolic allometry in animals by linking microevolutionary processes to macroevolutionary patterns. We show that the genetic correlation between mass and metabolic rate is strong and positive in insects, birds, and mammals. We then use these data to simulate the macroevolution of mass and metabolic rate, and show that the interspecific relationship between these traits in animals is consistent with evolution under persistent multivariate selection on mass and metabolic rate over long periods of time.
In variable environments, selection should favor generalists that maintain fitness across a range of conditions. However, costs of adaptation may generate fitness trade-offs and lead to some compromise between specialization and generalization that maximizes fitness. Here, we evaluate the evolution of specialization and generalization in 20 populations of Drosophila melanogaster experimentally evolved in constant and variable thermal environments for 3 years. We developed genotypes from each population at two temperatures after which we measured fecundity across eight temperatures. We predicted that constant environments would select for thermal specialists and that variable environments would select for thermal generalists. Contrary to our predictions, specialists and generalists did not evolve in constant and spatially variable environments, respectively. However, temporal variation produced a type of generalist that has rarely been considered by theoretical models of developmental plasticity. Specifically, genotypes from the temporally variable selective environment were more fecund across all temperatures than were genotypes from other environments. These patterns suggest certain allelic effects and should inspire new directions for modeling adaptation to fluctuating environments. K E Y W O R D S :Acclimation, experimental evolution, phenotypic plasticity, specialist-generalist trade-offs, thermal adaptation.
The effect of temperature on the evolution of metabolism has been the subject of debate for a century; however, no consistent patterns have emerged from comparisons of metabolic rate within and among species living at different temperatures. We used experimental evolution to determine how metabolism evolves in populations of Drosophila melanogaster exposed to one of three selective treatments: a constant 16°C, a constant 25°C, or temporal fluctuations between 16 and 25°C. We tested August Krogh's controversial hypothesis that colder environments select for a faster metabolism. Given that colder environments also experience greater seasonality, we also tested the hypothesis that temporal variation in temperature may be the factor that selects for a faster metabolism. We measured the metabolic rate of flies from each selective treatment at 16, 20.5, and 25°C. Although metabolism was faster at higher temperatures, flies from the selective treatments had similar metabolic rates at each measurement temperature. Based on variation among genotypes within populations, heritable variation in metabolism was likely sufficient for adaptation to occur. We conclude that colder or seasonal environments do not necessarily select for a faster metabolism. Rather, other factors besides temperature likely contribute to patterns of metabolic rate over thermal clines in nature.
Natural selection alters the distribution of a trait in a population and indirectly alters the distribution of genetically correlated traits. Long-standing models of thermal adaptation assume that trade-offs exist between fitness at different temperatures; however, experimental evolution often fails to reveal such trade-offs. Here, we show that adaptation to benign temperatures in experimental populations of Drosophila melanogaster resulted in correlated responses at the boundaries of the thermal niche. Specifically, adaptation to fluctuating temperatures (16–25°C) decreased tolerance of extreme heat. Surprisingly, flies adapted to a constant temperature of 25°C had greater cold tolerance than did flies adapted to other thermal conditions, including a constant temperature of 16°C. As our populations were never exposed to extreme temperatures during selection, divergence of thermal tolerance likely reflects indirect selection of standing genetic variation via linkage or pleiotropy. We found no relationship between heat and cold tolerances in these populations. Our results show that the thermal niche evolves by direct and indirect selection, in ways that are more complicated than assumed by theoretical models.
Ionizing radiation is used as a phytosanitary treatment to mitigate risks from invasive species associated with trade of fresh fruits and vegetables. Commodity producers prefer to irradiate fresh product stored in modified atmosphere packaging that increases shelf life and delays ripening. However, irradiating insects in low oxygen may increase radiation tolerance, and regulatory agencies are concerned modified atmosphere packaging will decrease efficacy of radiation doses. Here, we examined how irradiation in a series of oxygen conditions (0.1-20.9 kPa O2) alters radiotolerance of larvae and pupae of a model lepidopteran Trichoplusia ni (Hubner) (Diptera: Noctuidae). Irradiating in severe hypoxia (0.1 kPa O2) increased radiation tolerance of insects compared with irradiating in atmospheric oxygen (20.9 kPa O2). Our data show irradiating pharate adult pupae at 600 Gy in moderately severe hypoxia (5 kPa O2) increased adult emergence compared with irradiation in atmospheric oxygen (20.9 kPa O2). Our data also show that in one of the three temporal replicates, irradiating T. ni larvae in moderately severe hypoxia (5 kPa O2) can also increase radiotolerance at an intermediate radiation dose of 100 Gy compared with irradiating in atmospheric oxygen conditions, but not at higher or lower doses. We discuss implications of our results in this model insect for the current generic doses for phytosanitary irradiation, including the recently proposed 250 Gy generic dose for lepidioptera larvae, and temporary restriction on irradiating commodities in modified atmosphere packaging that reduces the atmosphere to < 18 kPa O2.
Summary 1.Exaggeration of male sexual ornaments should be costly, in terms of metabolic expenditure, resource allocation or even locomotor function. For example, many male ornaments are predicted to affect the aerodynamics, drag or biomechanics of movement and thus inhibit the speed or manoeuvrability of individuals; but empirical support for this is equivocal. 2. We tested the locomotor and metabolic costs of exaggerated male ornaments in the threadfin rainbowfish (Iriatherina werneri), an Australasian native fish characterized by excessively long fin streamers. We predicted that males with greater relative ornamentation would have reduced escape abilities (i.e. burst swim speeds) as well as higher metabolic costs when resting or swimming. Furthermore, we evaluated the benefits of the signal by comparing the preference of females for males with differing amounts of ornamentation. 3. As expected, we found that females spent more time observing (i.e. preferred) males with longer relative fins. We also experimentally reduced threadfin length and found that females continued to show preference for males with longer fins, rather than a preference for particular males. 4. Male I. werneri with longer ornaments had higher resting metabolic rates, but we found no effect of ornament size on metabolic rates during swimming. Males with longer threadfins tended to swim faster, but our manipulation of fin length had no effect on burst swimming speed, indicating swimming abilities are not causally related to threadfin length. 5. Overall, we found no evidence that the extravagant ornaments of male threadfin rainbowfish increase the metabolic or functional costs associated with swimming. Our results are surprising, given the high viscosity of water and the extreme length of I. werneri's ornaments. We suggest that future work should focus on the fitness costs of threadfin length, relative to reproductive output or survival under more natural conditions.
The most commonly assumed cost for exaggerated male ornamentation is increased predation pressure owing to decreased locomotor performance or increased conspicuousness to predators. Despite its intuitive basis, the locomotor costs of male ornamentation are not well established. We tested the hypothesis that multiple male signals that are used independently during female choice and male competition could lead to varied locomotor costs. Multiple signals with varied costs could provide a more detailed indicator of overall male quality, as only the highest-quality individuals could support all costs. To test this idea, we investigated the burst locomotor consequences of multiple ornaments for males of the pacific blue-eye (Pseudomugil signifer). We evaluated five competing models relating body size, ornament size and performance traits to field measures of dominance and attractiveness. Non-propulsive male fin ornaments used during male competition were different from those used in female choice. First dorsal fin length was the most important predictor of male attractiveness, while dominance was only associated with anal fin length. Furthermore, first dorsal fin length was positively correlated with swim speed, while anal fin length was negatively associated with speed. Our study shows that multiple male signals that are used independently during male competition and female choice also differ in their associated costs. This provides a mechanism for understanding why locomotor costs for exaggerated male ornamentation are not often empirically demonstrated.
SUMMARYOrganisms adjust to seasonal variability in the environment by responding to cues that indicate environmental change. As most studies of seasonal phenotypic plasticity test only the effect of a single environmental cue, how animals may integrate information from multiple cues to fine-tune plastic responses remains largely unknown. We examined the interaction between correlated (seasonally matching) and conflicting (seasonally opposite) temperature and photoperiod cues on the acclimation of performance traits in male zebrafish, Danio rerio. We acclimated fish for 8weeks and then tested the change in thermal dependence of maximum burst swimming and feeding rate between 8 and 38°C. We predicted that correlated environmental cues should induce a greater acclimation response than uncorrelated cues. However, we found that only temperature was important for the seasonal acclimation of performance traits in zebrafish. Thermal acclimation shifted the thermal performance curve of both traits. For maximum burst swimming, performance increased for each group near the acclimation temperature and reduced in environments that were far from their acclimation temperature. The feeding rate of cold-acclimated zebrafish was reduced across the test temperature range compared with that of warm-acclimated fish. Our study is the first that has found no effect of the covariation between temperature and photoperiod acclimation cues on locomotor performance in fishes. Our results support the intuitive idea that photoperiod may be a less important seasonal cue for animals living at lower latitudes.
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