Morphology,performance, fitness: functional insight into a post-Pleistocene radiation of mosquitofish

Bahamas mosquitofish (Gambusia hubbsi) colonized blue holes during the past approximately 15 000 years and exhibit relatively larger caudal regions in blue holes that contain piscivorous fish. It is hypothesized that larger caudal regions enhance fast-start escape performance and thus reflect an adaptation for avoiding predation. Here I test this hypothesis using a three-pronged, experimental approach. First, G. hubbsi from blue holes with predators were found to possess both greater fast-start performance and greater survivorship in the presence of predatory fish. Second, using individual-level data to investigate the morphology–performance–fitness pathway, I found that (i) fish with larger caudal regions produced higher fast-start performance and (ii) fish with higher fast-start performance enjoyed greater survivorship in the presence of fish predators—trends consistently observed across both predator regimes. Finally, I found that morphological divergence between predator regimes at least partially reflects genetic differentiation, as differences were retained in fish raised in a common laboratory environment. These results suggest that natural selection favours increased fast-start performance in the presence of piscivorous fish, consequently driving the evolution of larger caudal regions. Combined with previous work, this provides functional insight into body shape divergence and ecological speciation among Bahamian blue holes.     

Origins of female genital diversity: Predation risk and lock‐and‐key explain rapid divergence during an adaptive radiation

The study of male genital diversity has long overshadowed evolutionary inquiry of female genitalia, despite its nontrivial diversity. Here, we identify four nonmutually exclusive mechanisms that could lead to genital divergence in females, and potentially generate patterns of correlated male–female genital evolution: (1) ecological variation alters the context of sexual selection (“ecology hypothesis”), (2) sexually antagonistic selection (“sexual‐conflict hypothesis”), (3) female preferences for male genitalia mediated by female genital traits (“female‐choice hypothesis”), and (4) selection against inter‐population mating (“lock‐and‐key hypothesis”). We performed an empirical investigation of all four hypotheses using the model system of Bahamas mosquitofish inhabiting blue holes that vary in predation risk. We found unequivocal support for the ecology hypothesis, with females exhibiting a smaller genital opening in blue holes containing piscivorous fish. This is consistent with stronger postmating female choice/conflict when predators are present, but greater premating female choice in their absence. Our results additionally supported the lock‐and‐key hypothesis, uncovering a pattern of reproductive character displacement for genital shape. We found no support for the sexual conflict or female choice hypotheses. Our results demonstrate a strong role for ecology in generating female genital diversity, and suggest that lock‐and‐key may provide a viable cause of female genital diversification.     

Environmental drivers of demographics, habitat use, and behavior during a post-Pleistocene radiation of Bahamas mosquitofish (Gambusia hubbsi)

A fundamental goal of evolutionary ecology is to understand the environmental drivers of ecological divergence during the early stages of adaptive diversification. Using the model system of the post-Pleistocene radiation of Bahamas mosquitofish (Gambusia hubbsi) inhabiting blue holes, we used a comparative field study to examine variation in density, age structure, tertiary (adult) sex ratio, habitat use, as well as adult feeding and social behaviors in relation to environmental features including predation risk, interspecific competition, productivity (e.g. chlorophyll a, zooplankton density), and abiotic factors (e.g. salinity, surface diameter). The primary environmental factor associated with ecological differentiation in G. hubbsi was the presence of piscivorous fish. Gambusia hubbsi populations coexisting with predatory fish were less dense, comprised of a smaller proportion of juveniles, and were more concentrated in shallow, near-shore regions of blue holes. In addition to predation risk, the presence of a competitor fish species was associated with G. hubbsi habitat use, and productivity covaried with both age structure and habitat use. Feeding and social behaviors differed considerably between sexes, and both sexes showed behavioral differences between predator regimes by exhibiting more foraging behaviors in the absence of predators and more sexual behaviors in their presence. Males additionally exhibited more aggressive behaviors toward females in the absence of predators, but were more aggressive toward other males in the presence of predators. These results largely matched a priori predictions, and several findings are similar to trends in other related systems. Variation in predation risk appears to represent the primary driver of ecological differentiation in this system, but other previously underappreciated factors (interspecific competition, resource availability) are notable contributors as well. This study highlights the utility of simultaneously evaluating multiple environmental factors and multiple population characteristics within a natural system to pinpoint environmental drivers of ecological differentiation.     

EVOLUTION OF MALE COLORATION DURING A POST‐PLEISTOCENE RADIATION OF BAHAMAS MOSQUITOFISH (GAMBUSIA HUBBSI)

Sexual signal evolution can be complex because multiple factors influence the production, transmission, and reception of sexual signals, as well as receivers’ responses to them. To grasp the relative importance of these factors in generating signal diversity, we must simultaneously investigate multiple selective agents and signaling traits within a natural system. We use the model system of the radiation of Bahamas mosquitofish (Gambusia hubbsi) inhabiting blue holes to test the effects of resource availability, male body size and other life‐history traits, key aspects of the transmission environment, sex ratio, and predation risk on variation in multiple male color traits. Consistent with previous work examining other traits in this system, several color traits have repeatedly diverged between predation regimes, exhibiting greater elaboration in the absence of predators. However, other factors proved influential as well, with variation in resource levels, body size, relative testes size, and background water color being especially important for several color traits. For one prominent signaling trait, orange dorsal fins, we further confirmed a genetic basis underlying population differences using a laboratory common‐garden experiment. We illustrate a promising approach for gaining a detailed understanding of the many contributing factors in the evolution of multivariate sexual signals.     

Ecological speciation in Gambusia fishes

Although theory indicates that natural selection can facilitate speciation as a by-product, demonstrating ongoing speciation via this by-product mechanism in nature has proven difficult. We examined morphological, molecular, and behavioral data to investigate ecology's role in incipient speciation for a post-Pleistocene radiation of Bahamas mosquitofish (Gambusia hubbsi) inhabiting blue holes. We show that adaptation to divergent predator regimes is driving ecological speciation as a by-product. Divergence in body shape, coupled with assortative mating for body shape, produces reproductive isolation that is twice as strong between populations inhabiting different predator regimes than between populations that evolved in similar ecological environments. Gathering analogous data on reproductive isolation at the interspecific level in the genus, we find that this mechanism of speciation may have been historically prevalent in Gambusia. These results suggest that speciation in nature can result as a by-product of divergence in ecologically important traits, producing interspecific patterns that persist long after speciation events have completed.     

Predator-driven phenotypic diversification in Gambusia affinis

Predation is heterogeneously distributed across space and time, and is presumed to represent a major source of evolutionary diversification. In fishes, fast-starts--sudden, high-energy swimming bursts--are often important in avoiding capture during a predator strike. Thus, in the presence of predators, we might expect evolution of morphological features that facilitate increased fast-start speed. We tested this hypothesis using populations of western mosquitofish (Gambusia affinis) that differed in level of predation by piscivorous fish. Body morphology of G. affinis males, females, and juveniles diverged in a consistent manner between predatory environments. Fish collected from predator populations exhibited a larger caudal region, smaller head, more elongate body, and a posterior, ventral position of the eye relative to fish from predator-free populations. Divergence in body shape largely matched a priori predictions based on biomechanical principles, and was evident across space (multiple populations) and time (multiple years). We measured maximum burst-swimming speed for male mosquitofish and found that individuals from predator populations produced faster bursts than fish from predator-free populations (about 20% faster). Biomechanical models of fish swimming and intrapopulation morphology-speed correlations suggested that body shape differences were largely responsible for enhanced locomotor performance in fish from predator populations. Morphological differences also persisted in offspring raised in a common laboratory environment, suggesting a heritable component to the observed morphological divergence. Taken together, these results strongly support the hypothesis that divergent selection between predator regimes has produced the observed phenotypic differences among populations of G. affinis. Based on biomechanical principles and recent findings in other species, it appears that the general ecomorphological model described in this paper will apply for many aquatic taxa, and provide insight into the role of predators in shaping the body form of prey organisms.     

Selection on an antagonistic behavioral trait can drive rapid genital coevolution in the burying beetle,Nicrophorus vespilloides

Male and female genital morphology varies widely across many taxa, and even among populations. Disentangling potential sources of selection on genital morphology is problematic because each sex is predicted to respond to adaptations in the other due to reproductive conflicts of interest. To test how variation in this sexual conflict trait relates to variation in genital morphology we used our previously developed artificial selection lines for high and low repeated mating rates. We selected for high and low repeated mating rates using monogamous pairings to eliminate contemporaneous female choice and male–male competition. Male and female genital shape responded rapidly to selection on repeated mating rate. High and low mating rate lines diverged from control lines after only 10 generations of selection. We also detected significant patterns of male and female genital shape coevolution among selection regimes. We argue that because our selection lines differ in sexual conflict, these results support the hypothesis that sexually antagonistic coevolution can drive the rapid divergence of genital morphology. The greatest divergence in morphology corresponded with lines in which the resolution of sexual conflict over mating rate was biased in favor of male interests.     

Trade-off between steady and unsteady swimming underlies predator-driven divergence in Gambusia affinis

Differences in predation intensity experienced by organisms can lead to divergent natural selection, driving evolutionary change. Western mosquitofish (Gambusia affinis) exhibit larger caudal regions and higher burst-swimming capabilities when coexisting with higher densities of predatory fish. It is hypothesized that a trade-off between steady (constant-speed cruising; important for acquiring resources) and unsteady (rapid bursts and turns; important for escaping predators) locomotion, combined with divergent selection on locomotor performance (favouring steady swimming in high-competition scenarios of low-predation environments, but unsteady swimming in high-predation localities) has caused such phenotypic divergence. Here, I found that morphological differences had a strong genetic basis, and low-predation fish required less hydromechanical power during steady swimming, leading to increased endurance. I further found individual-level support for cause-and-effect relationships between morphology, swimming kinematics and endurance. Results indicate that mosquitofish populations inhabiting low-predation environments have evolved increased steady-swimming abilities via stiffer bodies, larger anterior body/head regions, smaller caudal regions and greater three-dimensional streamlining.     

Changes in sexual signals are greater than changes in ecological traits in a dichromatic group of fishes

Understanding the mechanisms by which phenotypic divergence occurs is central to speciation research. These mechanisms can be revealed by measuring differences in traits that are subject to different selection pressures; greater influence of different types of selection can be inferred from greater divergence in associated traits. Here, we address the potential roles of natural and sexual selection in promoting phenotypic divergence between species of snubnose darters by comparing differences in body shape, an ecologically relevant trait, and male color, a sexual signal. Body shape was measured using geometric morphometrics, and male color was measured using digital photography and visual system‐dependent color values. Differences in male color are larger than differences in body shape across eight allopatric, phylogenetically independent species pairs. While this does not exclude the action of divergent natural selection, our results suggest a relatively more important role for sexual selection in promoting recent divergence in darters. Variation in the relative differences between male color and body shape across species pairs reflects the continuous nature of speciation mechanisms, ranging from ecological speciation to speciation by sexual selection alone.     

Ontogenetic and evolutionary effects of predation and competition on nine-spined stickleback (Pungitius pungitius) body size

1.?Individual- and population-level variation in body size and growth often correlates with many fitness traits. Predation and food availability are expected to affect body size and growth as important agents of both natural selection and phenotypic plasticity. How differences in predation and food availability affect body size/growth during ontogeny in populations adapted to different predation and competition regimes is rarely studied. 2.?Nine-spined stickleback (Pungitius pungitius) populations originating from habitats with varying levels of predation and competition are known to be locally adapted to their respective habitats in terms of body size and growth. Here, we studied how different levels of perceived predation risk and competition during ontogeny affect the reaction norms of body size and growth in (i) marine and pond populations adapted to different levels of predation and competition and (ii) different sexes. We reared nine-spined stickleback in a factorial experiment under two levels of perceived predation risk (present/absent) and competition (high/low food supply). 3.?We found divergence in the reaction norms at two levels: (i) predation-adapted marine stickleback had stronger reactions to predatory cues than intraspecific competition-adapted pond stickleback, the latter being more sensitive to available food than the marine fish and (ii) females reacting more strongly to the treatments than males. 4.?The repeated, habitat-dependent nature of the differences suggests that natural selection is the agent behind the observed patterns. Our results suggest that genetic adaptation to certain environmental factors also involves an increase in the range of expressible phenotypic plasticity. We found support for this phenomenon at two levels: (i) across populations driven by habitat type and (ii) within populations driven by sex.     

Causes of male sexual trait divergence in introduced populations of guppies

Males from different populations of the same species often differ in their sexually selected traits. Variation in sexually selected traits can be attributed to sexual selection if phenotypic divergence matches the direction of sexual selection gradients among populations. However, phenotypic divergence of sexually selected traits may also be influenced by other factors, such as natural selection and genetic constraints. Here, we document differences in male sexual traits among six introduced Australian populations of guppies and untangle the forces driving divergence in these sexually selected traits. Using an experimental approach, we found that male size, area of orange coloration, number of sperm per ejaculate and linear sexual selection gradients for male traits differed among populations. Within populations, a large mismatch between the direction of selection and male traits suggests that constraints may be important in preventing male traits from evolving in the direction of selection. Among populations, however, variation in sexual selection explained more than half of the differences in trait variation, suggesting that, despite within‐population constraints, sexual selection has contributed to population divergence of male traits. Differences in sexual traits were also associated with predation risk and neutral genetic distance. Our study highlights the importance of sexual selection in trait divergence in introduced populations, despite the presence of constraining factors such as predation risk and evolutionary history.     

Quantitative traits and mode of speciation in Martinique anoles

We investigate extensive quantitative trait variation (dewlap hue, colour pattern, dorsum hue, body proportions and scalation) in the Martinique anole across eight transects representing nascent parapatric ecological speciation, nascent allopatric speciation and allopatric divergence without sufficient genetic structure to suggest speciation. Quantitative trait divergence can be extremely large between adjacent sets of populations, but with one exception that this is associated with difference in habitat rather than past allopatry. Nascent ecological speciation shows the greatest level of quantitative trait divergence across all character sets including those implicated in natural, as well as sexual selection. The sole example of nascent allopatric speciation is associated with fairly strong quantitative trait divergence among most character sets, but not the set most implicated in natural (rather than sexual) selection. The role of sexual selection in ecological speciation is discussed, both in terms of female choice with assortative mating and male–male competition with condition‐dependant sexual signals.     

Correlated divergence of female and male genitalia in replicated lineages with ongoing ecological speciation

Divergence of genital traits among lineages has the potential to serve as a reproductive isolating barrier when copulation, insemination, and fertilization are inhibited by incompatibilities between female and male genitalia. Despite widespread evidence for genital trait diversity among closely related lineages and coevolution of female and male genitalia within lineages, few studies have investigated genital evolution during the early stages of speciation. We quantified genital variation in replicated population pairs of Poecilia mexicana with ongoing ecological speciation between sulfidic (H₂S containing) and nearby nonsulfidic habitats. These analyses revealed rapid and correlated divergence of female and male genitalia across evolutionarily independent population pairs exposed to divergent selection regimes. Both sexes exhibited convergent evolution of genital traits among populations inhabiting similar habitat types. Our results demonstrate that genital evolution can occur during the early stages of speciation‐with‐gene‐flow, potentially as a result of variation in the intensity of sexual conflict among populations. Our results suggest genitalia may contribute to early stages of divergence and challenge the generality of previously suggested mechanisms of genital evolution in poeciliids.     

Evidence for stabilizing selection and slow divergent evolution of male genitalia in a millipede (Antichiropus variabilis)

It is generally accepted that postcopulatory sexual selection drives rapid divergence of genital morphology among isolated populations. The mode of selection operating upon genitalia can be explored by comparing patterns of population divergence in genetic and genitalic traits. We collected Antichiropus variabilis millipedes from eight localities across the species range. Levels of among-population genetic divergence, at microsatellite loci, and the mitochondrial COI gene were very high. Following geometric morphometric analyses, genital morphology was also found to be highly divergent among the populations surveyed, whereas head morphology had not diverged as markedly. However, pairwise comparisons of F(ST) and P(ST) showed that among-population divergence in both genital and head shape was significantly lower than that experienced by neutral genetic markers. Our results suggest that the genitalia of A. variabilis are currently experiencing a period of stabilizing selection, the mode of selection expected for genitalia that function in species recognition via a "lock-and-key" mechanism. Our results demonstrate that although genital morphology can clearly diverge among genetically isolated populations, divergence is not necessarily as rapid as commonly argued, and continuous directional sexual selection may not always underpin the evolutionary divergence of male genitalia.     

Intraspecific evidence from guppies for correlated patterns of male and female genital trait diversification

The role of sexual selection in fuelling genital evolution is becoming increasingly apparent from comparative studies revealing interspecific divergence in male genitalia and evolutionary associations between male and female genital traits. Despite this, we know little about intraspecific variance in male genital morphology, or how male and female reproductive traits covary among divergent populations. Here we address both topics using natural populations of the guppy, Poecilia reticulata, a livebearing fish that exhibits divergent patterns of male sexual behaviour among populations. Initially, we performed a series of mating trials on a single population to examine the relationship between the morphology of the male's copulatory organ (the gonopodium) and the success of forced matings. Using a combination of linear measurements and geometric morphometrics, we found that variation in the length and shape of the gonopodium predicted the success of forced matings in terms of the rate of genital contacts and insemination success, respectively. We then looked for geographical divergence in these traits, since the relative frequency of forced matings tends to be greater in high-predation populations. We found consistent patterns of variation in male genital size and shape in relation to the level of predation, and corresponding patterns of (co)variation in female genital morphology. Together, these data enable us to draw tentative conclusions about the underlying selective pressures causing correlated patterns of divergence in male and female genital traits, which point to a role for sexually antagonistic selection.     

Shift in predation regime mediates diversification of foraging behaviour in a dragonfly genus

1. Behavioural adaptations to avoid and evade predators are common. Many studies have investigated population divergence in response to changes in predation regime within species, but studies exploring interspecific patterns are scant. Studies on interspecific divergence can infer common outcomes from evolutionary processes and highlight the role of environmental constraints in shaping species traits. 2. Species of the dragonfly genus Leucorrhinia underwent well‐studied shifts from habitats being dominated by predatory fish (fish lakes) to habitat being dominated by predatory invertebrates (dragonfly lakes). This change in top predators resulted in a set of adaptive trait modifications in response to the different hunting styles of both predator types: whereas predatory fish actively search and pursue prey, invertebrate predator follow a sit‐and‐wait strategy, not pursuing prey. 3. Here it is shown that the habitat shift‐related change in selection regime on larval Leucorrhinia caused species in dragonfly lakes to evolve increased larval foraging and activity, and results suggest that they lost the ability to recognise predatory fish. 4. The results of the present study highlight the impact of predators on behavioural trait diversification with habitat‐specific predation regimes selecting for distinct behavioural expression.     

SPATIOTEMPORAL VARIATION IN LINEAR NATURAL SELECTION ON BODY COLOR IN WILD GUPPIES (POECILIA RETICULATA)

We conducted 10 mark–recapture experiments in natural populations of Trinidadian guppies to test hypotheses concerning the role of viability selection in geographic patterns of male color variation. Previous work has reported that male guppies are more colorful in low‐predation sites than in high‐predation sites. This pattern of phenotypic variation has been theorized to reflect differences in the balance between natural (viability) selection that disfavors bright male color (owing to predation) and sexual selection that favors bright color (owing to female choice). Our results support the prediction that male color is disfavored by viability selection in both predation regimes. However, it does not support the prediction that viability selection against male color is weaker in low‐predation experiments. Instead, some of the most intense bouts of selection against color occurred in low‐predation experiments. Our results illustrate considerable spatiotemporal variation in selection among experiments, but such variation was not generally correlated with local patterns of color diversity. More complex selective interactions, possibly including the indirect effects of predators on variation in mating behavior, as well as other environmental factors, might be required to more fully explain patterns of secondary sexual trait variation in this system.     

A benthic predatory fish does not cause selection on armour traits in three‐spined stickleback Gasterosteus aculeatus (Gasterosteiformes: Gasterosteidae)

Predation can promote divergence between prey populations and contribute to ecological speciation. In theory, predators can also constrain prey population divergence. In coastal British Columbia, Canada, Gasterosteus aculeatus (three‐spined stickleback) species pairs only occur in lakes with a single species of predatory fish: Oncorhynchus clarkii (the cutthroat trout). Similar lakes containing additional predatory fish species (Cottus asper, prickly sculpins; Oncorhynchus mykiss, rainbow trout) contain only single species of morphologically intermediate stickleback, suggesting that these predators prevent the coexistence of stickleback species pairs. We conducted a mesocosm experiment to investigate how prickly sculpins might constrain divergence, by quantifying their impact on survival and natural selection on antipredator (armour) traits in F₂ stickleback from a cross between ecologically divergent populations. We tested three hypotheses: (1) sculpin predation on sticklebacks reduces survival in a way that could result in their exclusion from certain niches; (2) sculpins compete with stickleback; (3) sculpins respond to prey vulnerabilities in similar ways to cutthroat trout, tending to constrain rather than to enhance divergence. We found that sculpins significantly reduce stickleback survival, that their presence per se does not reduce growth in stickleback, and that predation did not result in selection on any of the armour traits measured, or on gill raker length, which is an important trophic trait. These results tend to refute hypotheses (2) and (3), while supporting hypothesis (1). © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 877–885.     

Altered predation susceptibility of mosquitofish infected with Eustrongylides ignotus

Eustrongylides ignotus is a parasitic nematode whose definitive hosts are often piscivorous wading birds (Ciconiiformes). Several species of small fishes are intermediate hosts, while larger predatory fish may be paratenic (transport) hosts. We examined predation susceptibility of infected mosquitofish (Gambusia holbrooki) to three species of predatory fishes, including juvenile largemouth bass (Micropterus salminoides), warmouth (Lepomis gulosus), and bluegill (Lepomis macrochirus). A 250 L aquarium with removable plexiglass divider and remote observation windows was constructed. Aquatic macrophytes were placed in the tank to provide refuge for the fishes. Predatory fish were allowed to acclimate to one half of the tank, while one infected and one uninfected mosquitofish were placed in the other. The divider was removed and an observer recorded the number of capture attempts and time required for capture. Predators were observed for behavioral alterations for 4 days after ingestion of infected mosquitofish, then examined at necropsy. Infected prey were selected preferentially in 31 of 38 (82%) trials. The number of capture attempts was 2.7+/-0.2 (x +/- SE) for infected fish and 3.9+/-0.4 for uninfected fish. Mean time of capture was 12.4+/-1.6 min for infected fish and 21.7+/-2.9 for uninfected fish. Because of these differences, infected mosquitofish were more susceptible to predation (P < 0.01) than uninfected fish. Aberrant behavior including lethargy, convulsions, and buoyancy abnormalities was observed in eight (67%) predatory fish. At necropsy, larvae of E. ignotus were found in the coelomic cavity, viscera, and swim bladders of predators. Parasite-induced behavior modification of intermediate hosts may predispose them to predation by wading birds and thereby facilitate the transmission of this nematode in natural populations.