Ontogeny and sex alter the effect of predation on body shape in a livebearing fish: sexual dimorphism, parallelism, and costs of reproduction

Predation can cause morphological divergence among populations, while ontogeny and sex often determine much of morphological diversity among individuals. We used geometric morphometrics to characterize body shape in the livebearing fish Brachyrhaphis rhabdophora to test for interactions between these three major shape-determining factors. We assessed shape variation between juveniles and adults of both sexes, and among adults for populations from high- and low-predation areas. Shape differed significantly between predation regimes for all juveniles regardless of sex. As males grew and matured into adults, ontogenetic shape trajectories were parallel, thus maintaining shape differences in adult males between predation environments. However, shape of adult females between predation environments followed a different pattern. As females grew and matured, ontogenetic shape trajectories converged so that shape differences were less pronounced between mature females in predator and nonpredator environments. Convergence in female body shape may indicate a trade-off between optimal shape for predator evasion versus shape required for the livebearing mode of reproduction.     

Oxygen consumption of gestating femaleSebastes schlegeli: Estimating the reproductive costs of livebearing

Synopsis During gestation, live-bearing fishes incur physiological energy costs, including provision of energy and respiratory gases to the developing embryos and removal of waste products. Fecundity in the genusSebastes is high, and the ovaries represent a significant portion of the weight of gestating females. In this study, we compare oxygen consumption of gestating females with non-gestating females and males of kurosoi,Sebastes schlegeli, to estimate these costs. Oxygen consumption by pregnant females is significantly higher than that of males and immature females at similar sizes and weights. We estimate that a 1.5 kg gestating female consumes 68% more oxygen than a non-gestating fish during the 51.5-day period of gestation. Such an increase in oxygen consumption rates may have important implications to the metabolic scope of gestating alone, suggesting that costs of increased gill ventilation, ionic and osmotic regulation and cardiac output are relatively high. Such energetic costs represent a quantifiable expense of the viviparous mode of reproduction inSebastes as compared with oviparous species.     

Habitat predicts reproductive superfetation and body shape in the livebearing fish Poeciliopsis turrubarensis

Superfetation, the ability of females to simultaneously carry more than one brood at different developmental stages, is an unusual reproductive strategy that has independently evolved several times in the livebearing fish family Poeciliidae. Why this strategy has evolved remains uncertain. One hypothesis is that superfetation is a response to selective pressures that constrain the physical space within a female in which her offspring can develop. This hypothesis is reasonable, because superfetation should reduce the total volume needed to house developing embryos – that is, fewer large, fully developed embryos will be held by a superfetating female (with several broods at different developmental stages) than a non‐superfetating female (where all embryos reach a fully developed stage at the same time). In this study, we explore this ‘morphological constraint’ hypothesis of superfetation by examining the livebearing fish, Poeciliopsis turrubarensis. We found that populations vary markedly in degree of superfetation, with individuals carrying from two to four distinct broods across different geographic areas. These populations also occupy a range of habitat types: some populations occur in slow moving coastal rivers near the ocean, while other populations occur far inland in fast moving waters that drain steep mountain environments. In comparing populations from these two types of environments, we find a strong association between stream habitat type and the degree of superfetation within populations. Fish from inland populations have higher levels of superfetation than their coastal counterparts. In addition, geometric morphometric analysis revealed that inland populations are also more fusiform than fish from coastal locations. Combined, these two lines of evidence support the ‘morphological constraint’ hypothesis, and suggest that the life history strategy of superfetation could be driven by environmental pressures that favor a more streamlined phenotype.     

Roots, shoots and reproduction: sexual dimorphism in size and costs of reproductive allocation in an annual herb

Females tend to be smaller than males in woody dioecious plant species, but they tend to be larger in herbs. The smaller size of females in woody species has been attributed to higher reproductive costs, yet no satisfactory explanation has been provided for their larger size in herbs. Because herbs have higher nitrogen concentrations in their tissues than woody plants, and because pollen is particularly rich in nitrogen, we predicted that male growth would be more compromised by reproduction than female growth. To test this hypothesis, we conducted three experiments on the annual dioecious herb Mercurialis annua. First, we compared the timing of reproduction between males and females and found that males started flowering earlier than females; early flowering is expected to compromise growth more than later flowering. Second, we compared plants allowed to flower with those prevented from flowering by experimental debudding and found that males incurred a higher reproductive cost than females in terms of both biomass and, particularly, nitrogen. Third, we grew plants under varying levels of nitrogen availability and found that although sexual size dimorphism was unaffected by nitrogen, females, but not males, decreased their relative allocation to both roots and reproduction under high nitrogen availability. We propose that males deal with the high cost of pollen production in terms of nitrogen by allocating biomass to nitrogen-harvesting roots, whereas females pay for carbon-rich seeds and fruits by investing in photosynthetic organs. Sexual dimorphism would thus seem to be the outcome of allocation to above- versus below-ground sinks that supply resources (carbon versus nitrogen) limiting the female and male reproduction differentially.     

Behavioural asymmetry affects escape performance in a teleost fish

Escape performance is fundamental for survival in fish and most other animals. While previous work has shown that both intrinsic (e.g. size, shape) and extrinsic (e.g. temperature, hypoxia) factors can affect escape performance, the possibility that behavioural asymmetry may affect timing and locomotor performance in startled fish is largely unexplored. Numerous studies have found a relationship between brain lateralization and performance in several cognitive tasks. Here, we tested the hypothesis that behavioural lateralization may affect escape performance in a teleost, the shiner perch Cymatogaster aggregata. Escape responses were elicited by mechanical stimulation and recorded using high-speed video (250 Hz). A number of performance variables were analysed, including directionality, escape latency, turning rate and distance travelled within a fixed time. A lateralization index was obtained by testing the turning preference of each subject in a detour test. While lateralization had no effect on escape directionality, strongly lateralized fish showed higher escape reactivity, i.e. shorter latencies, which were associated with higher turning rates and longer distances travelled. Therefore, lateralization is likely to result in superior ability to escape from predator attacks, since previous work has shown that escape timing, turning rate and distance travelled are among the main determinants of escape success.     

Life history patterns of a livebearing fish in contrasting environments

Summary The population dynamics and energy allocations of the Gila topminnow, a small livebearing fish, were studied in two contrasting environments, a spring run of constant characteristics and a fluctuating desert wash. Topminnows grew and matured in two basic patterns. First, many fish in both areas matured the year after their birth. Second, spring fish born early in the breeding season grew rapidly, bred within five months, and died by eight months of age. Although spring fish assimilated more energy, wash fish actually expended more calories for growth and reproduction, partly because of lower maintenance costs. Reproductive effort of long-lived spring fish varied with age between 3.1 and 6.5%; whereas efforts of short-lived spring and wash fish increased steadily with age to 5.2 and 9.8%, respectively. Although spring fish produced eggs of higher energy content, females in both areas varied their investment per offspring, apparently tracking seasonal changes in the availability of food for fry. When long-lived spring fish experienced food shortage, they allocated less energy to both growth and reproduction; in contrast, wash and short-lived spring fish under similar conditions reduced only their growth allocation. The reproductive mass in spring fish appeared to be limited by food availability, incompletely filled the abdominal space, and reflected no tradeoff between fecundity and investment per offspring. Reproduction by wash fish appeared to be limited by body space and was characterized by a tradeoff between fecundity and egg size.     

Reproductive investment in relation to survival risk in a livebearing fish

Fish have comparatively small brains and are not renowned for their intelligence. Yet a series of laboratory experiments on the guppy reveals that they can be surprisingly good at learning from each other, and that social learning processes can mediate behavioural traditions analogous to the tool using traditions of different populations of chimpanzees. Transmission chain experiments have established that arbitrary and even maladaptive information can be socially transmitted among shoals of fish. Studies of behavioural innovation in guppies are strikingly consistent with findings of equivalent studies in primates. There are strong sex differences in innovatory tendencies and social learning abilities in guppies, which also parallel observations of primates. These studies suggest that the adage 'necessity is the mother of invention' may be a characteristic feature of animal innovation. When considered in combination with the findings of transfer experiments carried out on natural populations of fish, it becomes apparent that fish are an excellent model system for studies of animal social learning and culture.     

Individual variation in reproductive costs of reproduction: high-quality females always do better

1. Although life-history theory predicts substantial costs of reproduction, individuals often show positive correlations among life-history traits, rather than trade-offs. The apparent absence of reproductive costs may result from heterogeneity in individual quality. 2. Using detailed longitudinal data from three contrasted ungulate populations (mountain goats, Oreamnos americanus; bighorn sheep, Ovis canadensis; and roe deer, Capreolus capreolus), we assessed how individual quality affects the probability of detecting a cost of current reproduction on future reproduction for females. We used a composite measure of individual quality based on variations in longevity (all species), success in the last breeding opportunity before death (goats and sheep), adult mass (all species), and social rank (goats only). 3. In all species, high-quality females consistently had a higher probability of reproduction, irrespective of previous reproductive status. In mountain goats, we detected a cost of reproduction only after accounting for differences in individual quality. Only low-quality female goats were less likely to reproduce following years of breeding than of nonbreeding. Offspring survival was lower in bighorn ewes following years of successful breeding than after years when no lamb was produced, but only for low-quality females, suggesting that a cost of reproduction only occurred for low-quality females. 4. Because costs of reproduction differ among females, studies of life-history evolution must account for heterogeneity in individual quality.     

Migratory costs and contemporary evolution of reproductive allocation in male chinook salmon

Energetically demanding migrations may impact the resources available for reproductive trait development and activity, and hence favour evolution of new investment strategies for remaining resources. We conducted a large-scale experiment to evaluate the proximate cost of migration on male reproductive investment in chinook salmon (Oncorhynchus tshawytscha) and contemporary evolution of reproductive allocation. Experimentally induced differences in migratory costs (17 km inland and 17 m elevation vs. 100 km and 430 m) influenced dorsal hump size and upper jaw length, two traits influencing male mating success that are developed during migration. Longer migration also reduced tissue energy reserves available for competition and length of breeding life. Corresponding shifts in the balance between natural and sexual selection appear to have been responsible for heritable population divergence in secondary sexual trait investment, in approximately 26 generations, following colonization of spawning sites with different migratory demands.     

Interpreting reproductive allometry: Individual strategies of allocation explain size-dependent reproduction in plant populations

Size-dependent or allometric relationships between reproductive and vegetative size are extremely common in plant populations. Reproductive allometry where plant size differences are due to environmental variability has been interpreted both as an adaptive strategy of plant growth and allocation, and as the product of fixed developmental constraints. Patterns of development are crucial in defining reproductive allometry but development is not fixed across individuals. For example, environmental adversity (e.g. resource impoverishment) tends to favor reproduction at relatively small sizes – an adaptive response to environmental adversity. While small individuals may have lower reproductive output than large individuals, all plants should maximize their reproductive output and relative allocation to reproduction may be constant across sizes. Thus, where individual plants within a population initiate reproduction at different sizes, no significant reproductive allometry is an appropriate null expectation. Reproductive allometry occurs in plant populations where initiating reproduction at small sizes yields relatively high or low reproductive size at final development. Both of these outcomes are common in plant populations. Our interpretation of reproductive allometry combines previous adaptive and developmental constraint interpretations, and is the first to successfully explain the range of relationships in plant populations where relative allocation has been observed to increase, decrease or remain constant will increasing plant size.     

Reproductive allocation and the long-term costs of reproduction in Siparuna grandiflora, a dioecious neo-tropical shrub

1 Using a combination of observational and experimental approaches, both allocation of resources to reproduction (often called the direct cost of reproduction) and the subsequent long-term costs (the indirect, delayed or demographic cost) associated with reproductive allocation to male and female function in Siparuna grandiflora (Siparunaceae), a tropical dioecious shrub, were examined.
2 The objectives were to determine whether females allocate more biomass or nitrogen per reproductive episode than males, and whether there is a long-term cost of reproduction in terms of subsequent growth or reproduction for either sex. If there is no long-term cost of reproduction, then reproduction may be viewed as free in an evolutionary sense.
3 As is generally the case in dioecious species, females allocated more biomass and nitrogen to reproduction than males. Females also showed delayed costs of reproduction in terms of decreased growth and subsequent reproduction, whereas males did not.
4 The lack of measurable delayed costs in males suggests that with the evolution of dioecy, selection has reduced delayed costs of reproduction in S. grandiflora males. In contrast, females that were prevented from reproducing were able to re-allocate resources to growth, and produced more stem length on average than males. This re-allocation response may have evolved to reduce delayed costs of reproduction in females over time frames longer than that considered in the present study.     

Individual differences in reproductive costs examined using multi-state methods

1.?Trade-offs among life-history traits are common because individuals have to partition limited resources between multiple traits. Reproductive costs are generally assumed to be high, resulting in reduced survival and fecundity in the following year. However, it is common to find positive rather than negative correlations between life-history traits. 2.?Here, we use a data set from the individual-based study of red deer on the Isle of Rum to examine how these costs vary between individuals and at different ages, using multi-state mark-recapture methodology. 3.?Females that had reproduced frequently in the past incurred lower costs of reproduction in terms of survival in the following year and were more likely to reproduce in two consecutive years. Older individuals and those that had not reproduced frequently exhibited higher costs. 4.?These results highlight the importance of considering heterogeneity and individual quality when examining trade-offs and demonstrate the effectiveness of using detailed long-term data sets to explore life-history strategies using multi-state mark-recapture models.     

Density-dependent reproduction in the European rabbit: a consequence of individual response and age-dependent reproductive performance

Density dependence of reproduction has generally been proposed to be caused by habitat heterogeneity and by the individual response of reproductive output. However, a further mechanism might generate density dependence of average reproductive rates. High density situations might be associated with a high proportion of first-season breeders which often show a principally lower reproductive performance. We tested for the existence of the latter mechanism as well as for density-dependent individual changes of reproductive effort in a population of European rabbits living in a homogeneous grassland habitat. The study was conducted over a period of eleven years. Overall, a strong relationship between mean reproductive rates and the breeding density of females was apparent. All necessary conditions for the presence of a density-dependent effect caused by age-dependent reproduction were fulfilled: Fluctuations of breeding density were paralleled by variations in the proportion of one-year-old females. These one-year-old, first-season breeders showed a consistently lower reproductive performance than older females, which might be caused by their lower body mass and their lower social rank. However, we also found strong evidence for density-dependent response of individual reproductive effort: Individual changes in fecundity over successive years were explained by changes in the breeding density of females. The results suggest that density dependence of reproduction in European rabbits is due to an interaction of age-dependent reproductive performance together with short-term fluctuations in breeding density, and a density-dependent, individual based response of reproductive rates. We further conclude that the lower reproductive performance of first-season breeders in age-structured animal populations may contribute substantially to interannual, and under particular circumstances to density-dependent variations of mean reproductive rates.     

Prenatal light exposure affects development of behavioural lateralization in a livebearing fish

The existence of individual differences in handedness and other lateralized functions is an unresolved problem. Genetic factors account for only a small proportion of the variance but the contribution of environmental influences is still largely unexplored. In chicks and zebrafish the amount of environmental light reaching embryos during development greatly influences the lateralization of adults. To investigate whether a similar effect is present in livebearers, we measured behavioural lateralization in ten-day-old goldbelly topminnows born from females that have been maintained at high or low light intensities during pregnancy. Fish from high-light treatment were significantly lateralized in both visual and motor tests while fish exposed to low light intensities were not. As observed in chicks and zebrafish, the main consequence of light exposure was the alignment of the laterality of different individuals in the same direction. Lateralization is known to affect a number of fitness-related traits in topminnow and we suggest that light influence may be part of an adaptive mechanism allowing to adjust the developmental trajectories of offspring to the prevailing environmental conditions.     

An indigenous religious ritual selects for resistance to a toxicant in a livebearing fish

Human-induced environmental change can affect the evolutionary trajectory of populations. In Mexico, indigenous Zoque people annually introduce barbasco, a fish toxicant, into the Cueva del Azufre to harvest fish during a religious ceremony. Here, we investigated tolerance to barbasco in fish from sites exposed and unexposed to the ritual. We found that barbasco tolerance increases with body size and differs between the sexes. Furthermore, fish from sites exposed to the ceremony had a significantly higher tolerance. Consequently, the annual ceremony may not only affect population structure and gene flow among habitat types, but the increased tolerance in exposed fish may indicate adaptation to human cultural practices in a natural population on a very small spatial scale.     

Variation in behavioral traits across a broad latitudinal gradient in a livebearing fish

Evolutionary Ecology - Variation in animal behavior can have important consequences for ecological processes like mate choice, resource competition and invasive potential. Characterizing behavioral...     

Parental effects improve escape performance of juvenile reef fish in a high-CO2 world

Rising CO₂ levels in the oceans are predicted to have serious consequences for many marine taxa. Recent studies suggest that non-genetic parental effects may reduce the impact of high CO₂ on the growth, survival and routine metabolic rate of marine fishes, but whether the parental environment mitigates behavioural and sensory impairment associated with high CO₂ remains unknown. Here, we tested the acute effects of elevated CO₂ on the escape responses of juvenile fish and whether such effects were altered by exposure of parents to increased CO₂ (transgenerational acclimation). Elevated CO₂ negatively affected the reactivity and locomotor performance of juvenile fish, but parental exposure to high CO₂ reduced the effects in some traits, indicating the potential for acclimation of behavioural impairment across generations. However, acclimation was not complete in some traits, and absent in others, suggesting that transgenerational acclimation does not completely compensate the effects of high CO₂ on escape responses.     

Experimental evolution in Heterandria formosa, a livebearing fish: group selection on population size

Group selection has historically been an important and controversial subject in evolutionary biology. There is now a compelling body of evidence, both theoretical and experimental, that group selection not only can be effective, but can be effective in situations when individual selection is not. However, experiments in which true population-level traits have been shown to evolve in response to group selection are currently limited to two species of flour beetle in the genus Tribolium and RNA viruses. Here we report the results of an experiment wherein we imposed group selection via differential extinction for increased and decreased population size at 6-week intervals, a true population-level trait, in the poeciliid fish Heterandria formosa. In contrast to most other group selection experiments, we observed no evolutionary response after six rounds of group selection in either the up- or down-selected lines. Populational heritability for population size was low, if not actually negative. Our results suggest that group selection via differential extinction may be effective only if population sizes are very small and/or migration rates are low.