The relative effects of pace of life-history and habitat characteristics on the evolution of sexual ornaments: A comparative assessment.

Selection may favor greater investment into sexual ornaments when opportunities for future reproduction are limited, for example, under high adult mortality. However, predation, a key driver of mortality, typically selects against elaborate sexual ornaments. Here, we examine the evolution of sexual ornaments in killifishes, which have marked contrasts in life-history strategy among species and inhabit environments that differ in accessibility to aquatic predators. We first assessed if the size of sexual ornaments (unpaired fins) influenced swimming performance. Second, we investigated whether the evolution of larger ornamental fins is driven primarily by the pace of life-history (investment into current vs. future reproduction) or habitat type (a proxy for predation risk). We found that larger fins negatively affected swimming performance. Further, males from species inhabiting ephemeral habitats, with lower predation risk, had larger fins and greater sexual dimorphism in fin size, compared to males from more accessible permanent habitats. We show that enlarged ornamental fins, which impair locomotion, evolve more frequently in environments that are less accessible to predators, without clear associations to life-history strategy. Our results provide a rare link between the evolution of sexual ornaments, effects on locomotion performance, and natural selection on ornament size potentially through habitat differences in predation risk.

Fast life-histories are associated with larger brain size in killifishes.

The high energetic demands associated with the vertebrate brain are proposed to result in a trade-off between the pace of life-history and relative brain size. However, because both life-history and brain size also have a strong relationship with body size, any associations between the pace of life-history and relative brain size may be confounded by coevolution with body size. Studies on systems where contrasts in the pace of life-history occur without concordant contrasts in body size could therefore add to our understanding of the potential coevolution between relative brain size and life-history. Using one such system - 21 species of killifish - we employed a common garden design across two ontogenetic stages to investigate the association between relative brain size and the pace of life-history. Contrary to predictions, we found that relative brain size was larger in adult fast-living killifishes, compared to slow-living species. Although we found no differences in relative brain size between juvenile killifishes. Our results suggest that fast- and slow-living killifishes do not exhibit the predicted trade-off between brain size and life-history. Instead, fast and slow-living killifishes could differ in the ontogenetic timing of somatic versus neural growth or inhabit environments that differ considerably in cognitive demands.

Variation in developmental rates is not linked to environmental unpredictability in annual killifishes.

Comparative evidence suggests that adaptive plasticity may evolve as a response to predictable environmental variation. However, less attention has been placed on unpredictable environmental variation, which is considered to affect evolutionary trajectories by increasing phenotypic variation (or bet hedging). Here, we examine the occurrence of bet hedging in egg developmental rates in seven species of annual killifish that originate from a gradient of variation in precipitation rates, under three treatment incubation temperatures (21, 23, and 25°C). In the wild, these species survive regular and seasonal habitat desiccation, as dormant eggs buried in the soil. At the onset of the rainy season, embryos must be sufficiently developed in order to hatch and complete their life cycle. We found substantial differences among species in both the mean and variation of egg development rates, as well as species-specific plastic responses to incubation temperature. Yet, there was no clear relationship between variation in egg development time and variation in precipitation rate (environmental predictability). The exact cause of these differences therefore remains enigmatic, possibly depending on differences in other natural environmental conditions in addition to precipitation predictability. Hence, if species-specific variances are adaptive, the relationship between development and variation in precipitation is complex and does not diverge in accordance with simple linear relationships.

Adjustments of cardiac mitochondrial phenotype in a warmer thermal habitat is associated with oxidative stress in European perch, Perca fluviatilis.

Mitochondria are playing key roles in setting the thermal limits of fish, but how these organelles participate in selection mechanisms during extreme thermal events associated with climate warming in natural populations is unclear. Here, we investigated the thermal effects on mitochondrial metabolism, oxidative stress, and mitochondrial gene expression in cardiac tissues of European perch (Perca fluviatilis) collected from an artificially heated ecosystem, the "Biotest enclosure", and an adjacent reference area in the Baltic sea with normal temperatures (~ 23 °C and ~ 16 °C, respectively, at the time of capture in summer). Fish were sampled one month after a heat wave that caused the Biotest temperatures to peak at ~ 31.5 °C, causing significant mortality. When assayed at 23 °C, Biotest perch maintained high mitochondrial capacities, while reference perch displayed depressed mitochondrial functions relative to measurements at 16 °C. Moreover, mitochondrial gene expression of nd4 (mitochondrial subunit of complex I) was higher in Biotest fish, likely explaining the increased respiration rates observed in this population. Nonetheless, cardiac tissue from Biotest perch displayed higher levels of oxidative damage, which may have resulted from their chronically warm habitat, as well as the extreme temperatures encountered during the preceding summer heat wave. We conclude that eurythermal fish such as perch are able to adjust and maintain mitochondrial capacities of highly aerobic organs such as the heart when exposed to a warming environment as predicted with climate change. However, this might come at the expense of exacerbated oxidative stress, potentially threatening performance in nature.

Parental effects influence life history traits and covary with an environmental cline in common frog populations.

Across latitudinal clines, the juvenile developmental rates of ectotherms often covary with the length of the growing season, due to life-history trade-offs imposed by the time-constrained environments. However, as the start of the growing season often varies substantially across years, adaptive parental effects on juvenile developmental rates may mediate the costs of a delayed season. By employing a meta-analysis, we tested whether larval developmental rates across a latitudinal cline of the common frog (Rana temporaria) are affected by fluctuating onsets of breeding, across years. We predicted that larval developmental rate will be inversely related to the onset of breeding, and that northern populations will be more prone to shorten their developmental rate in response to late breeding, as the costs of delayed metamorphosis should be highest in areas with a shorter growing season. We found that the larval period of both northern and southern populations responded to parental environmental conditions to a similar degree in absolute terms, but in different directions. In northern populations, a late season start correlated with decreased development time, suggesting that the evolution of parental effects aids population persistence in time-constrained environments. In southern populations, late season start correlated with increased development time, which could potentially be explained as a predator avoidance strategy. Our findings suggest that local ecological variables can induce adaptive parental effects, but responses are complex, and likely trade-off with other ecological factors.

Cardiac mitochondrial plasticity and thermal sensitivity in a fish inhabiting an artificially heated ecosystem.

Some evidence suggests that cardiac mitochondrial functions might be involved in the resilience of ectotherms such as fish to environmental warming. Here, we investigated the effects of acute and chronic changes in thermal regimes on cardiac mitochondrial plasticity and thermal sensitivity in perch (Perca fluviatilis) from an artificially heated ecosystem; the "Biotest enclosure" (~25 °C), and from an adjacent area in the Baltic Sea with normal temperatures (reference, ~16 °C). We evaluated cardiac mitochondrial respiration at assay temperatures of 16 and 25 °C, as well as activities of lactate dehydrogenase (LDH) and citrate synthase (CS) in Biotest and reference perch following 8 months laboratory-acclimation to either 16 or 25 °C. While both populations exhibited higher acute mitochondrial thermal sensitivity when acclimated to their natural habitat temperatures, this sensitivity was lost when Biotest and reference fish were acclimated to 16 and 25 °C, respectively. Moreover, reference fish displayed patterns of metabolic thermal compensation when acclimated to 25 °C, whereas no changes were observed in Biotest perch acclimated to 16 °C, suggesting that cardiac mitochondrial metabolism of Biotest fish expresses local adaptation. This study highlights the adaptive responses of cardiac mitochondria to environmental warming, which can impact on fish survival and distribution in a warming climate.

Macroevolutionary evidence suggests trait-dependent coevolution between behavior and life-history.

Species with fast life-histories typically prioritize current over future reproductive events, compared to species with slow life-histories. These species therefore require greater energetic input into reproduction, and also likely have less time to realize their reproductive potential. Hence, behaviors that increase access to both resources and mating opportunities, at a cost of increased mortality risk, could coevolve with the pace of life-history. However, whether this prediction holds across species, remains untested under standardized conditions. Here, we test how risky behaviors, which facilitate access to resources and mating opportunities (i.e., activity, boldness, and aggression), along with metabolic rate, coevolve with the pace of life-history across 20 species of killifish that present remarkable divergences in the pace of life-history. We found a positive association between the pace of life-history and aggression, but interestingly not with other behavioral traits or metabolic rate. Aggression is linked to interference competition, and in killifishes is often employed to secure mates, while activity and boldness are more relevant for exploiting energetic resources. Our results suggest that the trade-off between current and future reproduction plays a more prominent role in shaping mating behavior, while behaviors related to energy acquisition may be influenced by ecological factors.

Environmental stress correlates with increases in both genetic and residual variances: A meta-analysis of animal studies.

Adaptive evolutionary responses are determined by the strength of selection and amount of genetic variation within traits, however, both are known to vary across environmental conditions. As selection is generally expected to be strongest under stressful conditions, understanding how the expression of genetic variation changes across stressful and benign environmental conditions is crucial for predicting the rate of adaptive change. Although theory generally predicts increased genetic variation under stress, previous syntheses of the field have found limited support for this notion. These studies have focused on heritability, which is dependent on other environmentally sensitive, but nongenetic, sources of variation. Here, we aim to complement these studies with a meta-analysis in which we examine changes in coefficient of variation (CV) in maternal, genetic, and residual variances across stressful and benign conditions. Confirming previous analyses, we did not find any clear direction in how heritability changes across stressful and benign conditions. However, when analyzing CV, we found higher genetic and residual variance under highly stressful conditions in life-history traits but not in morphological traits. Our findings are of broad significance to contemporary evolution suggesting that rapid evolutionary adaptive response may be mediated by increased evolutionary potential in stressed populations.