Functional consequences of phenotypic variation between locally adapted populations: Swimming performance and ventilation in extremophile fish

Natural selection drives the evolution of traits to optimize organismal performance, but optimization of one aspect of performance can influence other aspects of performance. Here, we asked how phenotypic variation between locally adapted fish populations affects locomotion and ventilation, testing for functional trade‐offs and trait–performance correlations. Specifically, we investigated two populations of livebearing fish (Poecilia mexicana) that inhabit distinct habitat types (hydrogen‐sulphide‐rich springs and adjacent nonsulphidic streams). For each individual, we quantified different metrics of burst swimming during simulated predator attacks, steady swimming and gill ventilation. Coinciding with predictions, we documented significant population differences in all aspects of performance, with fish from sulphidic habitats exhibiting higher steady swimming performance and higher ventilation capacity, but slower burst swimming. There was a significant functional trade‐off between steady and burst swimming, but not between different aspects of locomotion and ventilation. Although our findings about population differences in locomotion performance largely parallel the results from previous studies, we provide novel insights about how morphological variation might impact ventilation and ultimately oxygen acquisition. Overall, our analyses provided insights into the functional consequences of previously documented phenotypic variation, which will help to disentangle the effects of different sources of selection that may coincide along complex environmental gradients.     

Genetic divergence in morphology-performance mapping between Misty Lake and inlet stickleback

Different environments should select for different aspects of organismal performance, which should lead to correlated divergence in morphological traits that influence performance. The result should be genetic divergence in aspects of performance, morphology and associations ('maps') between morphology and performance. Testing this hypothesis requires quantifying performance and morphology in multiple populations after controlling for environmental differences, but this is rarely attempted. We used a common-garden experiment to examine morphology and several aspects of swimming performance within and between the lake and inlet populations of threespine stickleback (Gasterosteus aculeatus) from the Misty system, Vancouver Island, Canada. Controlling for body size, lake stickleback had shallower bodies, larger caudal fins and smaller pelvic girdles. With or without morphological covariates, lake stickleback showed greater performance in both sustained and burst swimming. In contrast, inlet stickleback showed greater manoeuverability than did lake stickleback in some analyses. Morphology-performance relationships were decoupled when considering variation within vs. between populations. Moreover, morphology-performance mapping differed between the two populations. Based on these observations, we advance a hypothesis for why populations adapting to different environments should show adaptive genetic divergence in morphology-performance mapping.     

EVOLUTION OF INTRINSIC GROWTH AND ENERGY ACQUISITION RATES. I. TRADE-OFFS WITH SWIMMING PERFORMANCE IN MENIDIA MENIDIA

Abstract Latitudinal populations of the Atlantic silverside, Menidia menidia , show substantial genetic variation in rates of energy acquistion and allocation. Reared in common environments, silversides from northern latitudes consume more food, grow faster and more efficiently, store more energy, and produce greater quantities of eggs than their southern conspecifics. The persistence of seemingly inferior southern genotypes in the face of ostensibly superior northern genotypes suggest that there are hidden evolutionary trade-offs associated with these elevated acquisition and allocation rates. We tested the hypothesis that rapid growth and high levels of food consumption trade-off against locomotory performance in M. menidia . We compared both aerobic (prolonged and endurance) and anaerobic (burst) swimming capacities between intrinsically fast-growing fish from the north (Nova Scotia, NS) and intrinsically slow-growing fish from the south (South Carolina, SC) and between growth-manipulated phenotypes within each population. We also compared swimming speeds and endurance between fasted and recently fed fish within populations. Maximum prolonged and burst swimming speeds of NS fish were significantly lower than those of SC fish, and swimming speeds of fast-growing phenotypes were lower than those of slow-growing phenotypes within populations. Fed fish had lower burst speeds and less endurance than fasted fish from the same population. Thus, high rates of growth and the consumption of large meals clearly diminish swimming performance, which likely increases vulnerability to predation and decreases survival and relative fitness. The submaximal growth rate of southern M. menidia appears to be adaptive, resulting from balancing selection on rates of somatic growth.     

Swimming performance and morphology of juvenile sockeye salmon, <Emphasis Type="Italic">Oncorhynchus nerka</Emphasis>: comparison of inlet and outlet fry populations

We raised two populations of sockeye salmon fry from fertilized eggs in the laboratory and tested the hypothesis that outlet fry populations, fish which must migrate upstream to reach rearing lakes after yolk-sac absorption, have better swimming ability and morphological characteristics conducive to enhanced swimming performance than inlet fry populations, fish which migrate downstream to rearing lakes. Despite being of identical age, fry from the outlet population were larger (approx. 6.7% longer, ~5 mm on average) and more laterally compressed than inlet fry at the time of our initial experiments. Using an open-top box flume, we found that the burst-swimming performance (in cm s⁻¹) of the outlet population was 31% better. We found no differences between populations in prolonged-swimming performance. We were unable to find any direct relationships between measures of swimming performance and size or shape variables, suggesting that the larger, more robust morphology of outlet fry was not responsible for the superior burst ability. Recent biochemical studies indicate outlet fry may be metabolically better provisioned for burst swimming than inlet fry. It is possible that the morphological differences between the populations of fry reflect adaptations needed by adults during their migration and spawning.     

Sex‐specific genetic differences in endurance swimming of Trinidadian guppies

Swim performance is considered a main fitness‐determining trait in many aquatic organisms. Swimming is generally the only way most aquatic prey can escape predation, and swimming capacity is directly linked to food capture, habitat shifts, and reproduction. Therefore, evolutionary studies of swim performance are important to understand adaptation to aquatic environments. Most studies, however, concentrate on the importance of burst‐swim responses to predators, and little is known about its effect on endurance. Even fewer studies associate differences in organism swim capabilities to key gender‐specific responses. In this experiment, we assess the gender‐specific genetic basis of swimming endurance among four different populations of Trinidadian guppies adapted to different predation regimes. Our results show that second‐generation common‐garden females adapted to a low‐predation environment show longer swim endurance than fish adapted to a high‐predation environment. We also find an expected effect of lowered swimming endurance during pregnancy, but interestingly, it did not matter whether the females were in advanced stages of pregnancy, which severely changes body morphology, versus mid‐pregnancy. Males did not show the same trends across populations, and overall had lower swim endurances than female fish combined even when accounting for size differences. Populations recently transplanted from high‐ to low‐predation environments showed similar endurance to natural low‐predation environments in one population but not the other. This study highlights the importance of endurance in the adaptation of aquatic organisms to different predation regimes.     

Interacting effects of predation risk and resource level on escape speed of amphibian larvae along a latitudinal gradient

Fast‐growing genotypes living in time‐constrained environments are often more prone to predation, suggesting that growth‐predation risk trade‐offs are important factors maintaining variation in growth along climatic gradients. However, the mechanisms underlying how fast growth increases predation‐mediated mortality are not well understood. Here, we investigated if slow‐growing, low‐latitude individuals have faster escape swimming speed than fast‐growing high‐latitude individuals using common frog (Rana temporaria) tadpoles from eight populations collected along a 1500 km latitudinal gradient. We measured escape speed in terms of burst and endurance speeds in tadpoles raised in the laboratory at two food levels and in the presence and absence of a predator (Aeshna dragonfly larvae). We did not find any latitudinal trend in escape speed performance. In low food treatments, burst speed was higher in tadpoles reared with predators but did not differ between high‐food treatments. Endurance speed, on the contrary, was lower in high‐food tadpoles reared with predators and did not differ between treatments at low food levels. Tadpoles reared with predators showed inducible morphology (increased relative body size and tail depth), which had positive effects on speed endurance at low but not at high food levels. Burst speed was positively affected by tail length and tail muscle size in the absence of predators. Our results suggest that escape speed does not trade‐off with fast growth along the latitudinal gradient in R. temporaria tadpoles. Instead, escape speed is a plastic trait and strongly influenced by the interaction between resource level and predation risk.     

黑斑侧褶蛙蝌蚪断尾后的补偿生长和发育研究

动物在经历不利的生长条件或环境后往往出现补偿生长。研究了黑斑侧褶蛙(Pelophylax nigromaculatus)蝌蚪经历来自食蚊鱼(Gambusia affinis)捕食造成断尾损伤后的补偿生长模式、断尾损失对蝌蚪游泳能力以及变态时间与大小的影响。结果表明,经历捕食压力后,全尾组和1/3断尾组蝌蚪的体长显著大于1/2断尾组蝌蚪的体长,全尾组和1/3断尾组之间的蝌蚪体长差异不显著;第19天时,1/2断尾组蝌蚪经过补偿生长后体长显著大于全尾组蝌蚪,1/3断尾组与全尾组和1/2断尾组之间的蝌蚪体长差异均不显著;三个实验组之间蝌蚪尾长差异不显著;全尾组蝌蚪的疾游速显著大于1/2断尾组蝌蚪的疾游速,1/3断尾组蝌蚪的疾游速与全尾组和1/2断尾组之间差异不显著,表明严重断尾对蝌蚪疾游速产生了消极影响。三个实验组蝌蚪的变态时间和变态前后形态差异均不显著。黑斑侧褶蛙蝌蚪能够在变态前调整生长轨迹补偿早期捕食风险造成的生长损失,断尾损失并不影响变态时间与大小,断尾超过一半的蝌蚪经过补偿生长后仍要付出一定的运动代价。     

Changing the habitat: the evolution of intercorrelated traits to escape from predators

Burst escape speed is an effective and widely used behaviour for evading predators, with burst escape speed relying on several different morphological features. However, we know little about how behavioural and underlying morphological attributes change in concert as a response to changes in selective predation regime. We studied intercorrelated trait differentiation of body shape and burst‐swim‐mediating morphology in response to a habitat shift‐related reduction in burst escape speed using larvae of the dragonfly genus Leucorrhinia. Species in this genus underwent a well‐known habitat shift from predatory fish lakes (fish lakes) to predatory fish‐free lakes dominated by large predatory dragonflies (dragonfly lakes) accompanied by relaxed selection on escape burst speed. Results revealed that species from fish lakes that possess faster burst speed have evolved a suite of functionally intercorrelated traits, expressing a wider abdomen, a higher abdominal muscles mass and a larger branchial chamber compared with species from dragonfly lakes. In contrast, populations within species did not show significant differences in muscle mass and branchial chamber size between lake types in three of the species. High multicollinearity among variables suggests that traits have evolved in concert rather than independently when Leucorrhinia shifted from fish lakes to dragonfly lakes. Thus, relaxed selection on burst escape speed in dragonfly‐lake species resulted in a correlated reduction of abdominal muscles and a smaller branchial chamber, likely to save production and/or maintenance costs. Our results highlight the importance of studying integrated behavioural and morphological traits to fully understand the evolution of complex phenotypes.     

Sex differences in compensatory and catch-up growth in the mosquitofish Gambusia holbrooki

In many taxa, temporary nutritional shortage early in development can favour compensatory strategies that include elevated growth (‘compensatory growth’) and/or extension of the usual period of development (‘catch-up growth’) once conditions improve. The net gains from each strategy depend on the extent to which larger body size increases fitness relative to associated costs (e.g. long-term effects on adult performance, or a greater risk of juvenile mortality). These costs and benefits are likely to differ between the sexes due to sex-specific selection. We documented the responses of male and female mosquitofish (Gambusia holbrooki) to 3 weeks of low food availability (7–28 days old) that restricted subsequent growth and morphology compared to control fish continuously reared on a high food diet (N = 635 fish total). Neither sex elevated their growth rate immediately after being returned to a normal diet compared to control fish. When measured over the entire period until maturation, however, females showed compensatory growth. Males did not. Both sexes also exhibited catch-up growth but the delay until maturation was significantly longer for males. Despite early growth restriction, both sexes eventually matured at almost the same size as control fish, although males had a significantly smaller gonopodium (a sexually selected trait) than that of control males. Reasons for these sex differences are discussed.     

Effect of growth compensation on subsequent physical fitness in green swordtails Xiphophorus helleri

Early environmental conditions have been suggested to influence subsequent locomotor performance in a range of species, but most measurements have been of initial (baseline) performance. By manipulating early growth trajectories in green swordtail fish, we show that males that underwent compensatory growth as juveniles had a similar baseline swimming endurance when mature adults to ad libitum fed controls. However, they had a reduced capacity to increase endurance with training, which is more likely to relate to Darwinian fitness. Compensatory growth may thus result in important locomotor costs later in life.     

Quantitative analysis of compensatory and catch-up growth in diverse taxa

1.?'Compensatory growth' and 'catch-up growth' are often used interchangeably to describe the faster than optimal growth that occurs following a period of dietary restriction in the development of many animals. Concerns about the statistical analysis of these studies have drawn attention to the risk of false detection in reports of compensatory and catch-up growth. 2.?This study aims to quantify the degree to which these compensatory responses occur across the animal kingdom. In addition, this study distinguishes the two terms, 'compensatory growth' and 'catch-up growth', to clarify the fitness consequences of rapid growth. Compensatory growth refers to a faster than usual growth rate, while catch-up growth implies attainment of control size. 3.?Eight meta-analyses and meta-regression analyses were conducted on data extracted from 88 papers, including 11 taxonomic classes. The results confirmed that both growth tactics (i.e. compensatory and catch-up growth) occur across a wide range of taxa and result in decreased direct fitness components. 4.?Importantly, the meta-analytic methods used made it possible to identify the specific experimental techniques that most successfully promoted rapid growth after restriction and key differences in the responses of the four major groups (mammals, birds, fish and arthropods) to dietary restriction. Endotherms are more likely to show a compensatory growth response because of their determinate growth; in contrast, the indeterminate and saltatory growth tactics of fish and arthropods reduce the pressure to rapidly achieve a large size. 5.?Among the first meta-analyses to be conducted in this field, this study provides valuable support for the premises of compensatory and catch-up growth and also discusses weaknesses in experimental design, and possible solutions, in compensatory growth research. For example, we recommend conducting the experiment within the most linear phase of an animal's growth to avoid analytical complications arising from size-dependent growth, and our results indicate that dietary dilution more closely resembles quantitative restriction than clutch size and intermittent feeding restriction methods when normal quantitative restriction is not possible.     

Locomotion at –1.0°C: burst swimming performance of five species of Antarctic fish

We investigated the burst swimming performance of five species of Antarctic fish at −1.0°C. The species studied belonged to the suborder, Notothenioidei, and from the families, Nototheniidae and Bathydraconidae. Swimming performance of the fish was assessed over the initial 300 ms of a startle response using surgically attached miniature accelerometers. Escape responses in all fish consisted of a C-type fast start; consisting of an initial pronounced bending of the body into a C-shape, followed by one or more complete tail-beats and an un-powered glide. We found significant differences in the swimming performance of the five species of fish examined, with average maximum swimming velocities (U_max) ranging from 0.91 to 1.39 m s⁻¹ and maximum accelerations (A_max) ranging from 10.6 to 15.6 m s⁻². The cryopelagic species, Pagothenia borchgrevinki, produced the fastest escape response, reaching a U_max and A_max of 1.39 m s⁻¹ and 15.6 m s⁻², respectively. We also compared the body shapes of each fish species with their measures of maximum burst performance. The dragonfish, Gymnodraco acuticeps, from the family Bathdraconidae, did not conform to the pattern observed for the other four fish species belonging to the family Nototheniidae. However, we found a negative relationship between buoyancy of the fish species and burst swimming performance.     

Thermal acclimation of interactions: differential responses to temperature change alter predator-prey relationship

Different species respond differently to environmental change so that species interactions cannot be predicted from single-species performance curves. We tested the hypothesis that interspecific difference in the capacity for thermal acclimation modulates predator-prey interactions. Acclimation of locomotor performance in a predator (Australian bass, Macquaria novemaculeata) was qualitatively different to that of its prey (eastern mosquitofish, Gambusia holbrooki). Warm (25°C) acclimated bass made more attacks than cold (15°C) acclimated fish regardless of acute test temperatures (10-30°C), and greater frequency of attacks was associated with increased prey capture success. However, the number of attacks declined at the highest test temperature (30°C). Interestingly, escape speeds of mosquitofish during predation trials were greater than burst speeds measured in a swimming arena, whereas attack speeds of bass were lower than burst speeds. As a result, escape speeds of mosquitofish were greater at warm temperatures (25°C and 30°C) than attack speeds of bass. The decline in the number of attacks and the increase in escape speed of prey means that predation pressure decreases at high temperatures. We show that differential thermal responses affect species interactions even at temperatures that are within thermal tolerance ranges. This thermal sensitivity of predator-prey interactions can be a mechanism by which global warming affects ecological communities.     

Compensatory growth strategies are affected by the strength of environmental time constraints in anuran larvae

Organisms normally grow at a sub-maximal rate. After experiencing a period of arrested growth, individuals often show compensatory growth responses by modifying their life-history, behaviour and physiology. However, the strength of compensatory responses may vary across broad geographic scales as populations differ in their exposition to varying time constraints. We examined differences in compensatory growth strategies in common frog (Rana temporaria) populations from southern and northern Sweden. Tadpoles from four populations were reared in the laboratory and exposed to low temperature to evaluate the patterns and mechanisms of compensatory growth responses. We determined tadpoles’ growth rate, food intake and growth efficiency during the compensation period. In the absence of arrested growth conditions, tadpoles from all the populations showed similar (size-corrected) growth rates, food intake and growth efficiency. After being exposed to low temperature for 1 week, only larvae from the northern populations increased growth rates by increasing both food intake and growth efficiency. These geographic differences in compensatory growth mechanisms suggest that the strategies for recovering after a period of growth deprivation may depend on the strength of time constraints faced by the populations. Due to the costs of fast growth, only populations exposed to the strong time constraints are prone to develop fast recovering strategies in order to metamorphose before conditions deteriorate. Understanding how organisms balance the cost and benefits of growth strategies may help in forecasting the impact of fluctuating environmental conditions on life-history strategies of populations likely to be exposed to increasing environmental variation in the future.     

中华绒螯蟹幼蟹温度选择与偏好研究

研究通过利用自动化的电子穿梭系统研究长江野生中华绒螯蟹幼蟹的行为参数对温度变化的响应, 进行了Ⅰ组8℃和14℃实验组、Ⅱ组14℃和21℃实验组、Ⅲ组21℃和28℃实验组、Ⅳ组28℃和35℃实验组共4个实验组。实验表明中华绒螯蟹幼蟹的最佳偏好温度在28℃。幼蟹会加速逃离不适温度区域, 且偏离温度越高游泳速率越高, 温度和游泳速率拟合方程: y=0.0027x2–0.1045x+1.5875, R2=0.8615, 昼夜(P>0.05)和雌雄性别(P>0.05)差异对温度的偏好选择未见明显影响。研究为中华绒螯蟹养殖、利用及野外环境下种群保护与调控管理提供科学依据。     

Divergence in pollen performance between Clarkia sister species with contrasting mating systems supports predictions of sexual selection

Animal taxa that differ in the intensity of sperm competition often differ in sperm production or swimming speed, arguably due to sexual selection on postcopulatory male traits affecting siring success. In plants, closely related self‐ and cross‐pollinated taxa similarly differ in the opportunity for sexual selection among male gametophytes after pollination, so traits such as the proportion of pollen on the stigma that rapidly enters the style and mean pollen tube growth rate (PTGR) are predicted to diverge between them. To date, no studies have tested this prediction in multiple plant populations under uniform conditions. We tested for differences in pollen performance in greenhouse‐raised populations of two Clarkia sister species: the predominantly outcrossing C. unguiculata and the facultatively self‐pollinating C. exilis. Within populations of each taxon, groups of individuals were reciprocally pollinated (n = 1153 pollinations) and their styles examined four hours later. We tested for the effects of species, population, pollen type (self vs. outcross), the number of competing pollen grains, and temperature on pollen performance. Clarkia unguiculata exhibited higher mean PTGR than C. exilis; pollen type had no effect on performance in either taxon. The difference between these species in PTGR is consistent with predictions of sexual selection theory.     

Reductions in prolonged swimming capacity following freshwater colonization in multiple threespine stickleback populations

We compared ancestral anadromous-marine and nonmigratory, stream-resident threespine stickleback (Gasterosteus aculeatus) populations to examine the outcome of relaxed selection on prolonged swimming performance. We reared marine and stream-resident fish from two locations in a common environment and found that both stream-resident populations had lower critical swimming speeds (U(crits) ) than marine populations. F1 hybrids from the two locations displayed significant differences in dominance, suggesting that the genetic basis for variation in U(crit) differs between locations. To determine which traits evolved in conjunction with, and may underlie, differences in performance capacity we measured a suite of traits known to affect prolonged swimming performance in fish. Although some candidate traits did not evolve (standard metabolic rate and two body shape traits), multiple morphological (pectoral fin size, shape, and four body shape measures) and physiological (maximum metabolic rate; MMR) traits evolved in the predicted direction in both stream-resident populations. However, data from F1 hybrids suggested that only one of these traits (MMR) had dominance effects similar to those of U(crit) in both locations. Overall, our data suggest that reductions in prolonged swimming performance were selected for in nonmigratory populations of threespine stickleback, and that decreases in MMR may mediate these reductions in performance.     

Effects of substrate roughening on the swimming performance of Schizothorax wangchiachii (Fang, 1936) in the Heishui River: Implications for vertical slot fishway design

Re-establishing the natural connectivity of rivers using fishways may mitigate the unfavourable effects of dam construction on riverine biodiversity and freshwater fish populations. Knowledge of the swimming performance of target species in specific regions is critical for designing fishways with a high passage efficiency. Substrate roughening with river stones of fishways is considered to improve fish swimming capacity by benefiting from reduced-velocity zones with lower energetic costs. However, the effectiveness of rough substrates in energy metabolism is rarely tested. We investigated the effect of substrate roughening on the swimming capacity, oxygen consumption and behaviour of Schizothorax wangchiachii from the Heishui River in a flume-type swimming respirometer. The results showed that substrate roughening improved critical and burst swimming speed by ~12.9% and ~15.0%, respectively, compared to the smooth substrate. Our results demonstrate that increased reduced-velocity zones, lowered metabolic rate and tail-beat frequency support our hypothesis that lower energetic costs improve fish swimming performance in rough substrate compared to smooth treatment. The traversable flow velocity model predicted that maximum traversable flow velocity and maximum ascent distance were higher over rough compared to smooth substrate fishways. Fishway substrate roughening may be a practical approach to improve fish swimming upstream for demersal riverine fish.     

Social status, access to food, and compensatory growth in juvenile Atlantic salmon

Juvenile Atlantic salmon Salmo salar subjected to three weeks of cooler temperatures were 8·5% smaller than controls at the end of the temperature manipulation, but had caught up in size 20 weeks later. The behavioural means is examined by which this catch-up or compensatory growth is achieved. While on average compensating fish did not spend more time feeding, dominant fish within each group gained more exclusive access to the feeding area during periods of catch-up growth. Therefore the extent to which compensatory growth could be achieved was dependent on both the social status of the individual and the dominants' ability to monopolize the food patch.