The Fish Family Poeciliidae as a Model to Study the Evolution and Diversification of Regenerative Capacity in Vertebrates

The capacity of regenerating a new structure after losing an old one is a major challenge in the animal kingdom. Fish have emerged as an interesting model to study regeneration due to their high and diverse regenerative capacity. To date, most efforts have focused on revealing the mechanisms underlying fin regeneration, but information on why and how this capacity evolves remains incomplete. Here, we propose the livebearing fish family Poeciliidae as a promising new model system to study the evolution of fin regeneration. First, we review the current state of knowledge on the evolution of regeneration in the animal kingdom, with a special emphasis on fish fins. Second, we summarize recent advances in our understanding of the mechanisms behind fin regeneration in fish. Third, we discuss potential evolutionary pressures that may modulate the regenerative capacity of fish fins and propose three new theories for how natural and sexual selection can lead to the evolution of fin regeneration: (1) signaling-driven fin regeneration, (2) predation-driven fin regeneration, and (3) matrotrophy-suppressed fin regeneration. Finally, we argue that fish from the family Poeciliidae are an excellent model system to test these theories, because they comprise of a large variety of species in a well-defined phylogenetic framework that inhabit very different environments and display remarkable variation in reproductive traits, allowing for comparative studies of fin regeneration among closely related species, among populations within species or among individuals within populations. This new model system has the potential to shed new light on the underlying genetic and molecular mechanisms driving the evolution and diversification of regeneration in vertebrates.

Consuming Costly Prey: Optimal Foraging and the Role of Compensatory Growth

Some prey are exceptionally difficult to digest, and yet even non-specialized animals may consume them—why? Durophagy, the consumption of hard-shelled prey, is thought to require special adaptations for crushing or digesting the hard shells to avoid the many potential costs of this prey type. But many animals lacking specializations nevertheless include hard-bodied prey in their diets. We describe several non-mutually exclusive adaptive mechanisms that could explain such a pattern, and point to optimal foraging and compensatory growth as potentially having widespread importance in explaining costly-prey consumption. We first conducted a literature survey to quantify the regularity with which non-specialized teleost fishes consume hard-shelled prey: stomach-content data from 325 teleost fish species spanning 82 families (57,233 stomach samples) demonstrated that non-specialized species comprise ~75% of the total species exhibiting durophagy, commonly consuming hard-shelled prey at low to moderate levels (~10–40% as much as specialists). We then performed a diet survey to assess the frequency of molluscivory across the native latitudinal range of a small livebearing fish, Gambusia holbrooki, lacking durophagy specializations. Molluscivory was regionally widespread, spanning their entire native latitudinal range (>14° latitude). Third, we tested for a higher frequency of molluscivory under conditions of higher intraspecific resource competition in Bahamian mosquitofish (Gambusia spp.). Examining over 5,300 individuals, we found that molluscivory was more common in populations with higher population density, suggesting that food limitation is important in eliciting molluscivory. Finally, we experimentally tested in G. holbrooki whether molluscivory reduces growth rate and whether compensatory growth follows a period of molluscivory. We found that consumption of hard-shelled gastropods results in significantly reduced growth rate, but compensatory growth following prior snail consumption can quickly mitigate growth costs. Our results suggest that the widespread phenomenon of costly-prey consumption may be partially explained by its relative benefits when few alternative prey options exist, combined with compensatory growth that alleviates temporary costs.

Predator Environment Does Not Predict Life History in the Morphologically Constrained Fish Alfaro cultratus (Cyprinodontiformes: Poeciliidae)

Predation is known to have a significant effect on life history diversification in a variety of species. However, physical constraints of body shape and size can sometimes limit life history divergence. We test this idea in the Costa Rican livebearing fish Alfaro cultratus. Individuals in this species have a narrow body and keeled ventral surface, and females do not develop a distended abdomen when pregnant like other livebearing fishes. Here, we describe the life history of A. cultratus from 20 different populations across both high-predation and low-predation environments. We found significantly lower reproductive allotment in females from high-predation environments than in females from low-predation environments, but no significant difference in female or male size at maturity, number of offspring produced by females, or size of offspring. We found that A. cultratus exhibit isometric patterns of allocation for clutch dry mass in relation to female dry mass in high-predation and low-predation environments. Our results suggest that body shape constraints in this species limit the life history divergence we typically see between populations from high-predation and low-predation environments in other species.

Artificial Light at Night Alters the Physiology and Behavior of Western Mosquitofish (Gambusia affinis)

Human population growth and its associated effects on the environment contribute to the rapid decrease of biodiversity worldwide. Artificial light at night (ALAN) is an anthropogenic pollutant that is increasing with the spread of urbanization and may contribute to biodiversity declines. ALAN alters the migration patterns of birds, communication in frogs, and impacts reproduction, behavior, and physiology of multiple other taxa. However, most of the studies on ALAN are based on terrestrial systems, and overall, the effects of ALAN on freshwater organisms are poorly understood. We investigated how ALAN affects the physiology, behavior, and reproduction of a widespread, tolerant species of freshwater fish. Gambusia affinis are small livebearing fish often found in urban streams. We exposed groups of female G. affinis to either a natural light cycle or a constant 24-h light cycle (ALAN) in the laboratory for 60 days. In another experiment, we exposed female G. affinis to the same treatments in outdoor mesocosms for 32 days. We found that exposure to ALAN lowered glucose levels in the brain and decreased swimming activity, but had no effect on cortisol release rates, reproduction, survival, or growth. This research is strengthened by measuring multiple metrics in response to ALAN and by incorporating both a field and laboratory component which confirm similar results. These results suggest that this tolerant species of fish may behaviorally adjust to ALAN rather than modulate their endocrine stress response.

What Drives Life-History Variation in the Livebearing Fish Poeciliopsis prolifica? An Assessment of Multiple Putative Selective Agents

Life-history traits are directly linked to fitness, and therefore, can be highly adaptive. Livebearers have been used as models for understanding the evolution of life histories due to their wide diversity in these traits. Several different selective pressures, including population density, predation, and resource levels, can shape life-history traits. However, these selective pressures are usually considered independently in livebearers and we lack a clear understanding of how they interact in shaping life-history evolution. Furthermore, selective pressures such as interspecific competition are rarely considered as drivers of life-history evolution in poeciliids. Here we test the simultaneous effects of several potential selective pressures on life-history traits in the livebearing fish Poeciliopsis prolifica. We employ a multi-model inference approach. We focus on four known agents of selection: resource availability, stream velocity, population density, and interspecific competition, and their effect on four life-history traits: reproductive allocation, superfetation, number of embryos, and individual embryo size. We found that models with population density and interspecific competition alone were strongly supported in our data and, hence, indicated that these two factors are the most important selective agents for most life-history traits, except for embryo size. When population density and interspecific competition increase there is an increase in each of the three life-history traits (reproductive allocation, superfetation, and number of embryos). For individual embryo size, we found that all single-agent models were equivalent and it was unclear which selective agent best explained variation. We also found that models that included population density and interspecific competition as direct effects were better supported than those that included them as indirect effects through their influence on resource availability. Our study underscores the importance of interspecific competitive interactions on shaping life-history traits and suggests that these interactions should be considered in future life-history studies.

Does Asymmetrical Gonopodium Morphology Predict Lateralized Behavior in the Fish Xenophallus umbratilis?

Why bilaterally symmetrical organisms express handedness remains an important question in evolutionary biology. In some species, anatomical asymmetries have evolved that accompany behavioral handedness, yet we know remarkably little about causal links between asymmetric morphological traits and behavior. Here, we explore if a dextral or sinistral orientation of the male intromittent organ predicts side preferences in male behaviors. Our study addresses this question in the Costa Rican livebearing fish, Xenophallus umbratilis. This fish has a bilaterally symmetrical body plan, with one exception—the male anal fin (gonopodium), used to inseminate females, terminates with a distinct left- or right-handed corkscrew morphology. We used a detour assay to test males for side biases in approach behavior when exposed to four different stimuli (predator, potential mate, novel object, empty tank control). We found that left morph males preferred using their right eye to view potential mates, predators, and the control, and that right morph males preferred to use their left eye to view potential mates and predators, and their right eye to view the control. Males of both morphs displayed no eye bias when approaching the novel object. Our results suggest that there is a strong link between behavior and gonopodium orientation, with right and left morph males responding with opposite directional behaviors when presented with the same stimuli. This presents the intriguing possibility that mating preferences—in this case constrained by gonopodial morphology—could be driving lateralized decision making in a variety of non-mating behaviors.

Imminent risk of predation reduces the relative strength of postcopulatory sexual selection in the guppy

Fifty years of research on sperm competition has led to a very good understanding of the interspecific variation in sperm production traits. The reasons why this variation is often very large within populations have been less investigated. We suggest that the interaction between fluctuating environmental conditions and polyandry is a key phenomenon explaining such variation. We focus here on imminent predation risk (IPR). IPR impacts significantly several aspects of prey behaviour and reproduction, and it is expected to influence the operation of sexual selection before and after mating. We estimated the effect of IPR on the male opportunity for pre- and postcopulatory sexual selection in guppies ( Poecilia reticulata ), a livebearing fish where females prefer colourful males and mate multiply. We used a repeated-measures design, in which males were allowed to mate with different females either under IPR or in a predator-free condition. We found that IPR increased the total opportunity for sexual selection and reduced the relative contribution of postcopulatory sexual selection to male reproductive success. IPR is inherently variable and our results suggest that interspecific reproductive interference by predators may contribute towards maintaining the variation in sperm production within populations. This article is part of the theme issue ‘Fifty years of sperm competition'.

Limia mandibularis, a new livebearing fish (Cyprinodontiformes: Poeciliidae) from Lake Miragoane, Haiti

Limia mandibularis, a new livebearing fish of the family Poeciliidae is described from Lake Miragoane in southwestern Haiti on Hispaniola. The new species differs from all other species in the genus Limia by the presence of a well-developed lower jaw, the absence of preorbital and preopercular pores, and preorbital and preopercular canals forming an open groove each. The description of this new Limia species from Lake Miragoane confirms this lake as an important center of endemism for the genus with a total of nine described species so far.