Brachyrhaphis Rhabdophora Research Articles

Behavioral response to chemical cues from injured conspecifics in the livebearing fish, Brachyrhaphis rhabdophora

AbstractPredator–prey dynamics have led to a strong selection of prey's ability to detect and respond to information about the risk environment. Further, intrinsic factors, such as sex, may cause prey to perceive and respond to information differently. Chemical alarm cues from injured conspecifics are a classic example of how prey have evolved to use publicly available information to shape their behavior and enhance fitness, yet sex‐specific alarm reactions are rarely considered. The purpose of our study was to compare how males and females respond to conspecific chemical alarm cues in the livebearing fish species, Brachyrhaphis rhabdophora. Furthermore, we tested males and females from populations with a high‐ or low‐predation environment. Brachyrhaphis rhabdophora showed strong alarm reactions, but contrary to our predictions, showed limited variation due to sex or predation environment. We found that males and females from both populations displayed lower activity levels and increased their swimming depth when exposed to an alarm cue, despite variable and consistent baseline behaviors among individuals. These data further contribute to our understanding of what factors shape the evolution of behavioral responses to chemical alarm cues in fishes.

Predation history has no effect on lateralized behavior in Brachyrhaphis rhabdophora.

Evolutionary biologists have grown increasingly interested in laterality, a phenomenon where bilaterally symmetrical organisms show a side bias in some trait. Lateralized behavior is particularly interesting because it is not necessarily tied to morphological asymmetry. What causes lateralized behavior remains largely unknown, although previous research in fishes suggest that fish might favor one eye over another to view potential food sources, mates, and to assess predation risk. Here we test the hypothesis that a history of predation risk predicts lateralized behavior in the livebearing fish Brachyrhaphis rhabdophora. To do this, we used a detour assay to test for eye bias when a focal fish approached various stimuli (predator, potential mate, novel object, and empty tank control). Contrary to our predictions, we found no differences in lateralized behavior between fish from populations that co-occurred with fish predators relative to those that do not co-occur with predators. In fact, we found no evidence for behavioral lateralization at all in response to any of the stimuli. We explore several possible explanations for why lateralized behavior is absent in this species, especially considering a large body of work in other livebearing fishes that shows that lateralized behavior does occur.

Testes mass in the livebearing fish Brachyrhaphis rhabdophora (Poeciliidae) varies hypoallometrically with body size but not between predation environments.

In this study, we considered potential causes of variation in testis size in the livebearing fish Brachyrhaphis rhabdophora. We evaluated variation in testes mass among individual males and among populations that occupy different selective environments. First, we predicted that small males should allocate more to testes mass than large males (i.e., hypoallometric pattern) based on a sperm competition argument. Second, based on life history theory and associated differences in mortality rates between populations that coexist with many fish predators and those with few predators, we predicted that males in high‐predation environments should allocate more to testes mass than males in habitats with few predators. Our results showed that small males allocated proportionally more to testes mass than larger males (slope of testes mass to body mass was hypoallometric). However, there was no effect of predator environment on testes mass independent of body size differences. In this system, size‐specific patterns of reproductive allocation in males (hypoallometry) differ from that seen in females (hyperallometry). Allocation to testes mass may respond to differences in mortality rate through selection on body size.

Predation environment affects boldness temperament of neotropical livebearers.

Behavioral traits of individuals are important phenotypes that potentially interact with many other traits, an understanding of which may illuminate the evolutionary forces affecting populations and species. Among the five axes of temperament is the propensity to behave boldly in the presence of a perceived risk. To determine the effect of different predatorial regimes on boldness and fearfulness, we assessed the behavior of individuals in a novel portable swim chamber (i.e., forced open‐field test) by Brachyrhaphis rhabdophora (n = 633). We used an information theoretic framework to compare generalized (logistic) linear fixed‐effects models of predatorial regime (predator‐free [n = 6] and predator [n = 4] sites), sex, and standard length (SL). Fish from predator sites were much more fearful in the novel arena than fish from nonpredator sites. This varied by length, but not by sex. At 48 mm SL, fish from nonpredator sites were 4.9 times more likely to express bold behavior (ambulation) in the novel swim chamber as fish from predator sites. Probabilities of “ambulating” within the swim chamber increased with size for nonpredator sites and decreased with size for predator sites.

Repeated evolution of local adaptation in swimming performance: population-level trade-offs between burst and endurance swimming inBrachyrhaphisfreshwater fish

Specialization is fundamentally important in biology because specialized traits allow species to expand into new environments, in turn promoting population differentiation and speciation. Specialization often results in trade-offs between traits that maximize fitness in one environment but not others. Despite the ubiquity of trade-offs, we know relatively little about how consistently trade-offs evolve between populations when multiple sets of populations experience similarly divergent selective regimes. In the present study, we report a case study on Brachyrhaphis fishes from different predation environments. We evaluate apparent within/between population trade-offs in burst-speed and endurance at two levels of evolutionary diversification: high- and low-predation populations of Brachyrhaphis rhabdophora, and sister species Brachyrhaphis roseni and Brachyrhaphis terrabensis, which occur in high- and low-predation environments, respectively. Populations of Brachyrhaphis experiencing different predation regimes consistently evolved swimming specializations indicative of a trade-off between two swimming forms that are likely highly adaptive in the environment in which they occur. We show that populations have become similarly locally adapted at both levels of diversification, suggesting that swimming specialization has evolved rather rapidly and persisted post-speciation. Our findings provide valuable insight into how local adaptation evolves at different stages of evolutionary divergence.

Effects of predation environment and food availability on somatic growth in theLivebearingFishBrachyrhaphis rhabdophora(Pisces:Poeciliidae)

Variation in somatic growth rates is of great interest to biologists because of the relationship between growth and other fitness-determining traits, and it results from both genetic and environmentally induced variation (i.e. plasticity). Theoretical predictions suggest that mean somatic growth rates and the shape of the reaction norm for growth can be influenced by variation in predator-induced mortality rates. Few studies have focused on variation in reaction norms for growth in response to resource availability between high-predation and low-predation environments. We used juvenile Brachyrhaphis rhabdophora from high-predation and low-predation environments to test for variation in mean growth rates and for variation in reaction norms for growth at two levels of food availability in a common-environment experiment. To test for variation in growth rates in the field, we compared somatic growth rates in juveniles in high-predation and low-predation environments. In the common-environment experiment, mean growth rates did not differ between fish from differing predation environments, but the interaction between predation environment and food level took the form of a crossing reaction norm for both growth in length and mass. Fish from low-predation environments exhibited no significant difference in growth rate between high and low food treatments. In contrast, fish from high-predation environments exhibited variation in growth rates between high and low food treatments, with higher food availability resulting in higher growth rates. In the field, individuals in the high-predation environment grow at a faster rate than those in low-predation environments at the smallest sizes (comparable to sizes in the common-environment experiment). These data provide no evidence for evolved differences in mean growth rates between predation environments. However, fish from high-predation environments exhibited greater plasticity in growth rates in response to resource availability suggesting that predation environments may exhibit increased variation in food availability for prey fish and consequent selection for plasticity.

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.

Morphological convergence during pregnancy among predator and nonpredator populations of the livebearing fishBrachyrhaphis rhabdophora(Teleostei: Poeciliidae)

Predation can drive morphological divergence in prey populations, although examples of divergent selection are typically limited to nonreproductive individuals. In livebearing females, shape often changes drastically during pregnancy, reducing speed and mobility and enhancing susceptibility to predation. In the present study, we document morphological divergence among populations of nonreproductive female livebearing fish (Brachyrhaphis rhabdophora) in predator and nonpredator environments. We then test the hypothesis that shape differences among nonreproductive females are maintained among reproductive females between predator and nonpredator environments. Nonreproductive females in predator environments had larger caudal regions and more fusiform bodies than females in nonpredator environments; traits that are associated with burst speed in fish. Shape differences were maintained in reproductive females, although the magnitude of this difference declined relative to nonreproductive females, suggesting morphological convergence during pregnancy. Phenotypic change vector analysis revealed that females in predator environments became more similar to females in nonpredator environments in the transition from nonreproductive to reproductive. Furthermore, the level of reproductive allocation affected shape similarly between predator environments. These results suggest a life-history constraint on morphology, in which predator-driven morphological divergence among nonreproductive B. rhabdophora is not maintained at the same level during pregnancy. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104, 386–392. ADDITIONAL KEYWORDS: geometric morphometrics – life history – morphology – predation – trade-off.

Differential mortality drives life‐history evolution and population dynamics in the fish Brachyrhaphis rhabdophora

Life-history theory predicts that populations experiencing different levels of extrinsic mortality will evolve divergent reproductive strategies. Previous work in the live-bearing fish Brachyrhaphis rhabdophora shows that individuals from populations that occur with piscivorous fish mature earlier and at smaller sizes and have more and smaller offspring than fish from populations without predators. However, until now, there have been no data to demonstrate that differences in mortality rates actually exist between predator and predator-free sites. Here we present the results of a serial mark-recapture field study designed to estimate mortality rates in natural populations of B. rhabodophora from Costa Rica. We found that fish from predator environments experience higher overall mortality rates and proportionally higher adult mortality rates than fish from predator-free environments. We then ask what impact differences in mortality rates have on B. rhabdophora population dynamics. Using a population matrix modeling approach, we found that B. rhabdophora that co-occur with predators have population growth rates similar to those without predators and both have confidence intervals that span lambda = 1.0. However, elasticity analysis revealed that the most important life-history stages for population growth in predator environments are found early in life and include growth through early ontogenetic stages and survival as small adults; in contrast, the most important life-history stages for population growth in predator-free environments occur late in life, including survival once large juvenile and adult stages are reached. Hence, we demonstrate two important links between predation and population demography, one ecological due to the direct impacts of predator-induced mortality and the other expressed through predator-mediated reproductive adaptation.

Shared and unique features of evolutionary diversification.

A fundamental question in evolutionary biology asks whether organisms experiencing similar selective pressures will evolve similar solutions or whether historical contingencies dominate the evolutionary process and yield disparate evolutionary outcomes. It is perhaps most likely that both shared selective forces as well as unique histories play key roles in the course of evolution. Consequently, when multiple species face a common environmental gradient, their patterns of divergence might exhibit both shared and unique elements. Here we describe a general framework for investigating and evaluating the relative importance of these contrasting features of diversification. We examined morphological diversification in three species of livebearing fishes across a predation gradient. All species (Gambusia affinis from the United States of America, Brachyrhaphis rhabdophora from Costa Rica, and Poecilia reticulata from Trinidad) exhibited more elongate bodies, a larger caudal peduncle, and a relatively lower position of the eye in predator populations. This shared response suggests that common selective pressures generated parallel outcomes within three different species. However, each species also exhibited unique features of divergence, which might reflect phylogenetic tendencies, chance events, or localized environmental differences. In this system, we found that shared aspects of divergence were of larger magnitude than unique elements, suggesting common natural selective forces have played a greater role than unique histories in producing the observed patterns of morphological diversification. Assessing the nature and relative importance of shared and unique responses should aid in elucidating the relative generality or peculiarity in evolutionary divergence.

Variation between and within the sexes in body size preferences

Although it is often assumed that males and females have mating preferences for larger individuals of the other sex, potential underlying differences between male and female preferences for body size are not commonly investigated. Here, sexual differences in body size preferences are examined in the poeciliid fish, Brachyrhaphis rhabdophora. Females preferred larger males to smaller males, but preference did not appear to be affected by female size. One population-level analysis for males did not indicate an overall preference for larger females. A closer examination, however, revealed an effect of male size on preference; larger males preferred larger females, while smaller males preferred smaller females. It appears then that females, regardless of size, share a preference for large males, but males differ in their behaviour, depending on their body size. In addition, while the degree of difference in size between paired females did not appear to affect male preference, the degree of difference in size between paired males strongly affected female preference; the greater the difference, the more strongly females preferred the larger male. Thus, intersexual selection is found to operate in both sexes, but how it operates appears to differ. Intrasexual and intersexual differences in mating behaviour may be missed when evaluating population-wide preferences. That is, there can be underlying differences in how the sexes respond and the consequences of such differences should be considered when investigating mate choice. The results are considered in terms of the evolution of mating preferences, alternative mating strategies, assortative mating, the maintenance of trait variation in a population, and current methods to evaluate mating preferences.

Variation between and within the sexes in body size preferences

Although it is often assumed that males and females have mating preferences for larger individuals of the other sex, potential underlying differences between male and female preferences for body size are not commonly investigated. Here, sexual differences in body size preferences are examined in the poeciliid fish, Brachyrhaphis rhabdophora . Females preferred larger males to smaller males, but preference did not appear to be affected by female size. One population-level analysis for males did not indicate an overall preference for larger females. A closer examination, however, revealed an effect of male size on preference; larger males preferred larger females, while smaller males preferred smaller females. It appears then that females, regardless of size, share a preference for large males, but males differ in their behaviour, depending on their body size. In addition, while the degree of difference in size between paired females did not appear to affect male preference, the degree of difference in size between paired males strongly affected female preference; the greater the difference, the more strongly females preferred the larger male. Thus, intersexual selection is found to operate in both sexes, but how it operates appears to differ. Intrasexual and intersexual differences in mating behaviour may be missed when evaluating population-wide preferences. That is, there can be underlying differences in how the sexes respond and the consequences of such differences should be considered when investigating mate choice. The results are considered in terms of the evolution of mating preferences, alternative mating strategies, assortative mating, the maintenance of trait variation in a population, and current methods to evaluate mating preferences.

Life-history phenotypes in populations of Brachyrhaphis episcopi (Poeciliidae) with different predator communities.

Variation among populations in extrinsic mortality schedules selects for different patterns of investment in key life-history traits. We compared life-history phenotypes among 12 populations of the live-bearing fish Brachyrhaphis episcopi. Five populations co-occurred with predatory fish large enough to prey upon adults, while the other seven populations lacked these predators. At sites with large predatory fish, both sexes reached maturity at a smaller size. Females of small to average length that co-occurred with predators had higher fecundity and greater reproductive allotment than those from populations that lacked predators, but the fecundity and reproductive allotment of females one standard deviation larger than mean body length did not differ among sites. In populations with large predatory fish, offspring mass was significantly reduced. In each population, fecundity, offspring size and reproductive allotment increased with female body size. When controlling for maternal size, offspring mass and number were significantly negatively correlated, indicating a phenotypic trade-off. This trade-off was non-linear, however, because reproductive allotment still increased with brood size after controlling for maternal size. Similar differences in life-history phenotypes among populations with and without large aquatic predators have been reported for Brachyrhaphis rhabdophora in Costa Rica and Poecilia reticulata (a guppy) in Trinidad. This may represent a convergent adaptation in life-history strategies attributable to predator-mediated effects or environmental correlates of predator presence.

Divergent life histories among populations of the fish Brachyrhaphis rhabdophora: detecting putative agents of selection by candidate model analysis

Studies of natural selection in the wild almost always begin by examining patterns of association between phenotypic adaptations and environmental factors thought to shape evolutionary change. Unfortunately, many studies pay little attention to the effects of model selection on the evolutionary inferences drawn from such correlative data. In this study, I employed a candidate model analysis to examine four potential causes of life‐history evolution in the livebearing fish Brachyrhaphis rhabdophora. Combining factor analysis with path analysis, I constructed a nested set of 17 models that represent the hypothetical effects of four putative selective agents (mortality, density, resource availability, and habitat stability) on life‐history evolution in this species. These models represent both direct and indirect effects of selection on the life history. Using the Akaike Information Criterion to distinguish among models, I found that simple models that contained only single selective agents most parsimoniously explained life‐history divergence among 27 B. rhabdophora populations. Surprisingly, the four putative selective agents could not be distinguished, suggesting that the selective environment could be composed of a single selective agent confounded with other environmental factors, or could be composed of a suite of environmental factors that act in concert to shape the life history. In addition, comparisons among more complex models indicated that direct effects of selective agents appear to have primacy over combinations of indirect selective interactions in explaining intraspecific variation in B. rhabdophora life histories.

ADAPTIVE LIFE-HISTORY EVOLUTION IN THE LIVEBEARING FISH BRACHYRHAPHIS RHABDOPHORA: GENETIC BASIS FOR PARALLEL DIVERGENCE IN AGE AND SIZE AT MATURITY AND A TEST OF PREDATOR-INDUCED PLASTICITY

I document a genetic basis for parallel evolution of life-history phenotypes in the livebearing fish Brachyrhaphis rhabdophora from northwestern Costa Rica. In previous work, I showed that populations of B. rhabdophora that co-occur with predators attain maturity at smaller sizes than populations that live in predator-free environments. I also demonstrated that this pattern of phenotypic divergence in life histories was independently repeated in at least five isolated drainages. However, life-history phenotypes measured from wild-caught fish could be attributed to environmental effects rather than to genetic differences among populations. In the present study, I reared male fish from four populations (two that co-occur with predators and two from predator-free environments) under four sets of environmental conditions. The pattern of phenotypic divergence in maturation size documented in the field between populations collected from different predation environments persisted after two generations in the laboratory. I also found a genetic basis for differences between populations in the age at which males attain maturity and in growth rates. By rearing fish in four different common environments, I tested for phenotypic plasticity in male life-history traits in response to nonlethal exposure to predators. There was a significant delay in the onset of sexual maturity in fish exposed to predators relative to those in the control, but no differences among treatments in size at maturity or growth rates. These results, coupled with previous work on B. rhabdophora, demonstrate a repeated pattern of parallel evolutionary divergence among genetically isolated populations that is strongly associated with predation.

Hierarchical organization of genetic variation in the Costa Rican livebearing fish Brachyrhaphis rhabdophora (Poeciliidae)

I examined the geographic distribution of genetic variation in the livebearing freshwater fish Brachyrhaphis rhabdophora in northwestern Costa Rica as revealed by allozymes and mitochondrial DNA sequences. Allelic variability at 11 enzyme-coding loci surveyed across 12 localities revealed marked genetic differentiation among populations within drainages (0P= 0.36) and among drainages within regions (0D=0.17), but not between northern and southern geographic regions (0R=– 0.02). Allozyme variation was hierarchically organized such that populations found within stream drainages were more similar to each other than to populations found in adjacent drainages, a result confirmed by cluster analysis. In contrast to the allozyme data, there was extremely little DNA sequence variation among populations in the mitochondrial control region (3 variable nucleotide positions out of 444 bp examined). The difference in genetic divergence between allozyme and mtDNA markers was unexpected and is discussed in terms of biogeographical colonization events and a molecular selective swéep on the mitochondrial genome, both processes that could explain the lack of mitochondrial variability in this highly subdivided species.

Hierarchical organization of genetic variation in the Costa Rican livebearing fish Brachyrhaphis rhabdophora (Poeciliidae)

I examined the geographic distribution of genetic variation in the livebearing freshwater fishBrachyrhaphis rhabdophora in northwestern Costa Rica as revealed by allozymes and mitochondrial DNA sequences. Allelic variability at 11 enzyme-coding loci surveyed across 12 localities revealed marked genetic differentiation among populations within drainages (P=0.36) and among drainages within regions (D=0.17), but not between northern and southern geographic regions (R=−0.02). Allozyme variation was hierarchically organized such that populations found within stream drainages were more similar to each other than to populations found in adjacent drainages, a result confirmed by cluster analysis. In contrast to the allozyme data, there was extremely little DNA sequence variation among populations in the mitochondrial control region (3 variable nucleotide positions out of 444 bp examined). The difference in genetic divergence between allozyme and mtDNA markers was unexpected and is discussed in terms of biogeographical colonization events and a molecular selective sweep on the mitochondrial genome, both processes that could explain the lack of mitochondrial variability in this highly subdivided species.

Predation environment predicts divergent life-history phenotypes among populations of the livebearing fish Brachyrhaphis rhabdophora.

We document a strong association between predation environment and life-history phenotypes in the Costa Rican livebearing fish Brachyrhaphis rhabdophora. Populations that co-occurred with piscine predators attained maturity at a smaller size, and produced more, smaller offspring relative to populations from predator-free environments. These differences persisted over 3years and between wet and dry seasons within a year. Reproductive allotment did not differ between predation environments, but was greater in the wet season than in the dry season. We also examined the phenotypic covariance structure among life-history traits and found traits to be highly correlated. Based on life-history differences, discriminant analyses showed that populations could be neatly classified by predation category, and could be reasonably classified into wet and dry season categories. Finally, we found that the pattern of predator-associated life-history divergence in B. rhabdophora is remarkably similar to that of the taxonomically distinct Trinidadian guppy (Poecilia reticulata), possibly pointing to an evolutionary convergence between these two systems.

An Experimental Study on the Effects of Predation Risk and Feeding Regime on the Mating Behavior of the Water Strider

Influence du risque du a la presence de predateurs et a au jeune subit sur le taux d'accouplement et sur sa duree