Diversity of intraspecific patterns of brain region size covariation in fish.

Traits often do not evolve in isolation or vary independently of other traits. Instead, they can be affected by covariation, both within and across species. However, the importance of within species trait covariation and, critically, the degree to which it varies between species has yet to be thoroughly studied. Brain morphology is a trait of great ecological and behavioral importance, with regions that are hypothesized to vary in size based on behavioral and cognitive demands. Sizes of brain regions have also been shown to covary with each other across various taxa. Here we test the degree to which covariation in brain region sizes within species has been conserved across ten teleost fish species. These ten species span five orders, allowing us to examine how phylogenetic proximity influences similarities in intraspecific trait covariation. Our results showed a trend that similar patterns of brain region size covariation occur in more closely related species. Interestingly, there were certain brain region pairs that showed similar levels of covariation across all species regardless of phylogenetic distance, such as the telencephalon and optic tectum, while others, such as the olfactory bulb and the hypothalamus, varied more independently. Ultimately, the patterns of brain region covariation shown here suggest that evolutionary mechanisms or constraints can act on specific brain regions independently, and that these constraints can change over evolutionary time.

Evolutionary divergence of plasticity in brain morphology between ecologically divergent habitats of Trinidadian guppies.

Phenotypic plasticity is critical for organismal performance and can evolve in response to natural selection. Brain morphology is often developmentally plastic, affecting animal performance in a variety of contexts. However, the degree to which the plasticity of brain morphology evolves has rarely been explored. Here, we use Trinidadian guppies (Poecilia reticulata), which are known for their repeated adaptation to high-predation (HP) and low-predation (LP) environments, to examine the evolution and plasticity of brain morphology. We exposed second-generation offspring of individuals from HP and LP sites to 2 different treatments: predation cues and conspecific social environment. Results show that LP guppies had greater plasticity in brain morphology compared to their ancestral HP population, suggesting that plasticity can evolve in response to environmentally divergent habitats. We also show sexual dimorphism in the plasticity of brain morphology, highlighting the importance of considering sex-specific variation in adaptive diversification. Overall, these results may suggest the evolution of brain morphology plasticity as an important mechanism that allows for ecological diversification and adaptation to divergent habitats.

Disentangling genetic, plastic and social learning drivers of sex-specific foraging behaviour in Trinidadian guppies (Poecilia reticulata).

Evolutionary biologists have long been interested in parsing out the roles of genetics, plasticity and their interaction on adaptive trait divergence. Since males and females often have different ecological and reproductive roles, separating how their traits are shaped by interactions between their genes and environment is necessary and important. Here, we disentangle the sex-specific effects of genetic divergence, developmental plasticity, social learning and contextual plasticity on foraging behaviour in Trinidadian guppies (Poecilia reticulata) adapted to high- or low-predation habitats. We reared second-generation siblings from both predation regimes with or without predator chemical cues, and with adult conspecifics from either high- or low-predation habitats. We then quantified their foraging behaviour in water with and without predator chemical cues. We found that high-predation guppies forage more efficiently than low-predation guppies, but this behavioural difference is context-dependent and shaped by different mechanisms in males and females. Higher foraging efficiency in high-predation females is largely genetically determined, and to a smaller extent socially learned from conspecifics. However, in high-predation males, higher foraging efficiency is plastically induced by predator cues during development. Our study demonstrates sex-specific differences in genetic versus plastic responses in foraging behaviour, a trait of significance in organismal fitness and ecosystem dynamics.

Embracing the diversity in diverse warning signals.

Positive frequency-dependent selection should theoretically lead to monomorphic warning coloration. Instead, numerous examples of polymorphic warning signals exist. Biases - for example, in human perception - hinder our appreciation and research of understanding warning signal diversity. We propose strategies to counter such biases and objectively move our field forward.

Evolutionary divergence of developmental plasticity and learning of mating tactics in Trinidadian guppies.

Behavioural plasticity is a major driver in the early stages of adaptation, but its effects in mediating evolution remain elusive because behavioural plasticity itself can evolve. In this study, we investigated how male Trinidadian guppies (Poecilia reticulata) adapted to different predation regimes diverged in behavioural plasticity of their mating tactic. We reared F2 juveniles of high- or low-predation population origins with different combinations of social and predator cues and assayed their mating behaviour upon sexual maturity. High-predation males learned their mating tactic from conspecific adults as juveniles, while low-predation males did not. High-predation males increased courtship when exposed to chemical predator cues during development; low-predation males decreased courtship in response to immediate chemical predator cues, but only when they were not exposed to such cues during development. Behavioural changes induced by predator cues were associated with developmental plasticity in brain morphology, but changes acquired through social learning were not. We thus show that guppy populations diverged in their response to social and ecological cues during development, and correlational evidence suggests that different cues can shape the same behaviour via different neural mechanisms. Our study demonstrates that behavioural plasticity, both environmentally induced and socially learnt, evolves rapidly and shapes adaptation when organisms colonize ecologically divergent habitats.

La plasticidad conductual es un factor importante en las primeras fases de adaptación, pero se conocen poco sus efectos sobre la evolución porque la plasticidad conductual en sí puede evolucionar. En este estudio, investigamos cómo los machos del guppy de Trinidad (Poecilia reticulata) adaptados a regímenes de depredación diferentes, han divergido en la plasticidad de su táctica de apareamiento. Criamos juveniles provenientes de poblaciones de alta y baja depredación hasta segunda generación (F2) bajo diferentes combinaciones de señales sociales y de depredación, y evaluamos su comportamiento de apareamiento al llegar a la madurez sexual. Los machos de alta depredación aprendieron su táctica de apareamiento de sus conespecíficos adultos, mientras que los machos de baja depredación no. Los machos de alta depredación aumentaron su cortejo al ser expuestos a señales de depredadores durante su desarrollo; mientras que los machos de baja depredación redujeron su cortejo en respuesta a señales inmediatas de depredadores, pero tan solo cuando no fueron expuestos a tales señales durante el desarrollo. Los cambios conductuales observados inducidos por las señales de depredación están asociados con una plasticidad en el desarrollo de la morfología cerebral, pero los cambios adquiridos por aprendizaje social no. En conclusión, demostramos que las poblaciones de guppy han divergido en su respuesta a señales sociales y ecológicas durante su desarrollo, y mostramos evidencia correlativa que sugiere que diferentes tipos de señales pueden influenciar el mismo comportamiento via mecanismos neuronales diferentes. Nuestro estudio muestra que la plasticidad conductual, tanto inducida por el medio ambiente combo aprendida socialmente, evoluciona rápidamente e influencia la adaptación durante la colonización de hábitats ecológicamente divergentes.

Integrating neuroplasticity and evolution.

Neuroplasticity and evolutionary biology have been prominent fields of study for well over a century. However, they have advanced largely independently, without consideration of the benefits of integration. We propose a new framework by which researchers can begin to examine the evolutionary causes and consequences of neuroplasticity. Neuroplasticity can be defined as changes to the structure, function or connections of the nervous system in response to individual experience. Evolution can alter levels of neuroplasticity if there is variation in neuroplasticity traits within and between populations. Neuroplasticity may be favored or disfavored by natural selection depending on the variability of the environment and the costs of neuroplasticity. Additionally, neuroplasticity may affect rates of genetic evolution in many ways: for example, decreasing rates of evolution by buffering against selection or increasing them via the Baldwin effect, by increasing genetic variation or by incorporating evolved peripheral changes to the nervous system. These mechanisms can be tested using comparative and experimental approaches and by examining patterns and consequences of variation in neuroplasticity among species, populations and individuals.

Rapid evolution of diet choice in an introduced population of Trinidadian guppies.

Eco-evolutionary theory has brought an interest in the rapid evolution of functional traits. Among them, diet is an important determinant of ecosystem structure, affecting food web dynamics and nutrient cycling. However, it is largely unknown whether diet, or diet preference, has a hereditary basis and can evolve on contemporary timescales. Here, we study the diet preferences of Trinidadian guppies Poecilia reticulata collected from directly below an introduction site of fish transplanted from a high-predation environment into a low predation site where their densities and competition increased. Behavioural assays on F2 common garden descendants of the ancestral and derived populations showed that diet preference has rapidly evolved in the introduced population in only 12 years (approx. 36 generations). Specifically, we show that the preference for high-quality food generally found in high-predation guppies is lost in the newly derived low-predation population, who show an inertia toward the first encountered food. This result is predicted by theory stating that organisms should evolve less selective diets under higher competition. Demonstrating that diet preference can show rapid and adaptive evolution is important to our understanding of eco-evolutionary feedbacks and the role of evolution in ecosystem dynamics.

Heterozygote advantage and pleiotropy contribute to intraspecific color trait variability.

The persistence of intrapopulation phenotypic variation typically requires some form of balancing selection because drift and directional selection eventually erode genetic variation. Heterozygote advantage remains a classic explanation for the maintenance of genetic variation in the face of selection. However, examples of heterozygote advantage, other than those associated with disease resistance, are rather uncommon. Across most of its distribution, males of the aposematic moth Arctia plantaginis have two hindwing phenotypes determined by a heritable one locus-two allele polymorphism (genotypes: WW/Wy = white morph, yy = yellow morph). Using genotyped moths, we show that the presence of one or two copies of the yellow allele affects several life-history traits. Reproductive output of both males and females and female mating success are negatively affected by two copies of the yellow allele. Females carrying one yellow allele (i.e., Wy) have higher fertility, hatching success, and offspring survival than either homozygote, thus leading to strong heterozygote advantage. Our results indicate strong female contribution especially at the postcopulatory stage in maintaining the color polymorphism. The interplay between heterozygote advantage, yellow allele pleiotropic effect, and morph-specific predation pressure may exert balancing selection on the color locus, suggesting that color polymorphism may be maintained through complex interactions between natural and sexual selection.

Model Systems in Ecology, Evolution, and Behavior: A Call for Diversity in Our Model Systems and Discipline.

AbstractEcologists and evolutionary biologists are fascinated by life's variation but also seek to understand phenomena and mechanisms that apply broadly across taxa. Model systems can help us extract generalities from amid all the wondrous diversity, but only if we choose and develop them carefully, use them wisely, and have a range of model systems from which to choose. In this introduction to the Special Feature on Model Systems in Ecology, Evolution, and Behavior (EEB), we begin by grappling with the question, What is a model system? We then explore where our model systems come from, in terms of the skills and other attributes required to develop them and the historical biases that influence traditional model systems in EEB. We emphasize the importance of communities of scientists in the success of model systems-narrow scientific communities can restrict the model organisms themselves. We also consider how our discipline was built around one type of "model scientist"-a history still reflected in the field. This lack of diversity in EEB is unjust and also narrows the field's perspective, including by restricting the questions asked and talents used to answer them. Increasing diversity, equity, and inclusion will require acting at many levels, including structural changes. Diversity in EEB, in both model systems and the scientists who use them, strengthens our discipline.

Safety in Numbers: How Color Morph Frequency Affects Predation Risk in an Aposematic Moth.

AbstractPolymorphic warning signals in aposematic systems are enigmatic because predator learning should favor the most common form, creating positive frequency-dependent survival. However, many populations exhibit variation in warning signals. There are various selective mechanisms that can counter positive frequency-dependent selection and lead to temporal or spatial warning signal diversification. Examining these mechanisms and their effects requires first confirming whether the most common morphs are favored at both local and regional scales. Empirical examples of this are uncommon and often include potentially confounding factors, such as a lack of knowledge of predator identity and behavior. We tested how bird behavior influences the survival of three coexisting morphs of the aposematic wood tiger moth Arctia plantaginis offered to a sympatric predator (great tit Parus major) at different frequencies. We found that although positive frequency-dependent selection is present, its strength is affected by predator characteristics and varying prey profitability. These results highlight the need to understand predator foraging in natural communities with variable prey defenses in order to better examine how behavioral interactions shape evolutionary outcomes.

Geographic mosaic of selection by avian predators on hindwing warning colour in a polymorphic aposematic moth.

Warning signals are predicted to develop signal monomorphism via positive frequency-dependent selection (+FDS) albeit many aposematic systems exhibit signal polymorphism. To understand this mismatch, we conducted a large-scale predation experiment in four countries, among which the frequencies of hindwing warning coloration of the aposematic moth, Arctia plantaginis, differ. Here we show that selection by avian predators on warning colour is predicted by local morph frequency and predator community composition. We found +FDS to be the strongest in monomorphic Scotland and lowest in polymorphic Finland, where the attack risk of moth morphs depended on the local avian community. +FDS was also found where the predator community was the least diverse (Georgia), whereas in the most diverse avian community (Estonia), hardly any models were attacked. Our results support the idea that spatial variation in predator communities alters the strength or direction of selection on warning signals, thus facilitating a geographic mosaic of selection.

Rapid Changes in the Sex Linkage of Male Coloration in Introduced Guppy Populations.

Theory predicts that the sex linkage of sexually selected traits can influence the direction and rate of evolution and should itself evolve in response to sex-specific selection. Some studies have found intraspecific differences in sex linkage associated with differences in selection pressures, but we know nothing about how fast these differences can evolve. Here we show that introduced guppy populations showing rapid evolution of male coloration also show rapid changes in sex-linkage patterns. A comparison, using hormonal manipulations in females, of introduced populations of different ages suggests a consistent increase of autosomal or X-linked coloration 2 years after introduction from high- to low-predation environments. Twenty years after introduction, populations already show the same pattern of coloration inheritance typical of natural low-predation populations in similar habitats. These results highlight that the contemporary evolution of sexually selected traits ought to be studied in concert with contemporary changes in linkage relationships.

Selection analysis on the rapid evolution of a secondary sexual trait.

Evolutionary analyses of population translocations (experimental or accidental) have been important in demonstrating speed of evolution because they subject organisms to abrupt environmental changes that create an episode of selection. However, the strength of selection in such studies is rarely measured, limiting our understanding of the evolutionary process. This contrasts with long-term, mark-recapture studies of unmanipulated populations that measure selection directly, yet rarely reveal evolutionary change. Here, we present a study of experimental evolution of male colour in Trinidadian guppies where we tracked both evolutionary change and individual-based measures of selection. Guppies were translocated from a predator-rich to a low-predation environment within the same stream system. We used a combination of common garden experiments and monthly sampling of individuals to measure the phenotypic and genetic divergence of male coloration between ancestral and derived fish. Results show rapid evolutionary increases in orange coloration in both populations (1 year or three generations), replicating the results of previous studies. Unlike previous studies, we linked this evolution to an individual-based analysis of selection. By quantifying individual reproductive success and survival, we show, for the first time, that males with more orange and black pigment have higher reproductive success, but males with more black pigment also have higher risk of mortality. The net effect of selection is thus an advantage of orange but not black coloration, as reflected in the evolutionary response. This highlights the importance of considering all components of fitness when understanding the evolution of sexually selected traits in the wild.

Colour polymorphism torn apart by opposing positive frequency-dependent selection, yet maintained in space.

Polymorphic warning signals in aposematic species are enigmatic because predator learning and discrimination should select for the most common coloration, resulting in positive frequency-dependent survival selection. Here, we investigated whether differential mating success could create sufficiently strong negative frequency-dependent selection for rare morphs to explain polymorphic (white and yellow) warning coloration in male wood tiger moths (Parasemia plantaginis). We conducted an experiment in semi-natural conditions where we estimated mating success for both white and yellow male moths under three different morph frequencies. Contrary to expectations, mating success was positively frequency-dependent: white morph males had high relative fitness when common, likewise yellow morph males had high relative fitness when instead they were common. We hence built a model parameterized with our data to examine whether polymorphism can be maintained despite two sources of positive frequency dependence. The model includes known spatial variation in the survival advantage enjoyed by the yellow morph and assumes that relative mating success follows our experimentally derived values. It predicts that polymorphism is possible under migration for up to approximately 20% exchange of individuals between subpopulations in each generation. Our results suggest that differential mating success combined with spatial variation in predator communities may operate as a selection mosaic that prevents complete fixation of either morph.

Sex-specific genetic differences in endurance swimming of Trinidadian guppies.

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

Beyond lifetime reproductive success: the posthumous reproductive dynamics of male Trinidadian guppies.

In semelparous populations, dormant germ banks (e.g. seeds) have been proposed as important in maintaining genotypes that are adaptive at different times in fluctuating environments. Such hidden storage of genetic diversity need not be exclusive to dormant banks. Genotype diversity may be preserved in many iteroparous animals through sperm-storage mechanisms in females. This allows males to reproduce posthumously and increase the effective sizes of seemingly female-biased populations. Although long-term sperm storage has been demonstrated in many organisms, the understanding of its importance in the wild is very poor. We here show the prevalence of male posthumous reproduction in wild Trinidadian guppies, through the combination of mark-recapture and pedigree analyses of a multigenerational individual-based dataset. A significant proportion of the reproductive population consisted of dead males, who could conceive up to 10 months after death (the maximum allowed by the length of the dataset), which is more than twice the estimated generation time. Demographic analysis shows that the fecundity of dead males can play an important role in population growth and selection.

Predation-associated differences in sex linkage of wild guppy coloration.

Evolutionary theory predicts that the sex linkage of sexually selected traits can influence the direction and rate of evolutionary change, and also itself be subject to selection. Theory abounds on how sex-specific selection, mate choice, or other phenomena should favor different types of sex-linked inheritance, yet evidence in nature remains limited. Here, we use hormone assays in Trinidadian guppies to explore the extent to which linkage of male coloration differs among populations adapted to varying predation regimes. Results show there is consistently higher degree of X- and autosomal linkage in body coloration among populations adapted to low-predation environments. More strikingly, analyses of an introduced population of guppies from a high- to a low-predation environment suggest that this difference can change in 50 years or less.

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.