Evolutionary divergence in phenotypic plasticity shapes brain size variation between coexisting sunfish ecotypes.

Mechanisms that generate brain size variation and the consequences of such variation on ecological performance are poorly understood in most natural animal populations. We use a reciprocal-transplant common garden experiment and foraging performance trials to test for brain size plasticity and the functional consequences of brain size variation in Pumpkinseed sunfish (Lepomis gibbosus) ecotypes that have diverged between nearshore littoral and offshore pelagic lake habitats. Different age-classes of wild-caught juveniles from both habitats were exposed for 6 months to treatments that mimicked littoral and pelagic foraging. Plastic responses in oral jaw size suggested that treatments mimicked natural habitat-specific foraging conditions. Plastic brain size responses to foraging manipulations differed between ecotypes, as only pelagic sourced fish showed brain size plasticity. Only pelagic juveniles under 1 year-old expressed this plastic response, suggesting that plastic brain size responses decline with age and so may be irreversible. Finally, larger brain size was associated with enhanced foraging performance on live benthic but not pelagic prey, providing the first experimental evidence of a relationship between brain size and prey-specific foraging performance in fishes. The recent post-glacial origin of these ecotypes suggests that brain size plasticity can rapidly evolve and diverge in fish under contrasting ecological conditions.

Interspecific and intraspecific comparisons reveal the importance of evolutionary context in sunfish brain form divergence.

Habitats can select for specialized phenotypic characteristics in animals. However, the consistency of evolutionary responses to particular environmental conditions remains difficult to predict. One trait of great ecological importance is brain form, which is expected to vary between habitats that differ in their cognitive requirements. Here, we compared divergence in brain form and oral jaw size across a common littoral-pelagic ecological axis in two sunfishes at both the intraspecific and interspecific levels. Brain form differed between habitats at every level of comparison; however, divergence was inconsistent, despite consistent differences in oral jaw size. Pumpkinseed and bluegill species differed in cerebellum, optic tectum and olfactory bulb size. These differences are consistent with a historical ecological divergence because they did not manifest between littoral and pelagic ecotypes within either species, suggesting constraints on changes to these regions over short evolutionary time scales. There were also differences in brain form between conspecific ecotypes, but they were inconsistent between species. Littoral pumpkinseed had larger brains than their pelagic counterpart, and littoral bluegill had smaller telencephalons than their pelagic counterpart. Inconsistent brain form divergence between conspecific ecotypes of pumpkinseed and bluegill sharing a common littoral-pelagic habitat axis suggests that contemporary ecological conditions and historic evolutionary context interact to influence evolutionary changes in brain form in fishes.

Isolating the effects of ontogenetic niche shift on brain size development using pumpkinseed sunfish ecotypes.

A functional relationship between relative brain size and cognitive performance has been hypothesized. However, the influence of ontogenetic niche shifts on cognitive performance is not well understood. Increases in body size can affect niche use but distinguishing nonecologically relevant brain development from effects associated with ecology is difficult. If survival is enhanced by functional changes in ecocognitive performance over ontogeny, then brain size development should track ontogenetic shifts in ecology. We control for nonecologically relevant brain size development by comparing brain growth between two ecotypes of Pumpkinseed sunfish whose ecologies diverge over ontogeny from a shared juvenile niche. Brain size differs between ecotypes from their birth year onwards even though their foraging ecology appears to diverge at age 3. This finding suggests that the eco-cognitive requirements of adult niches shape early life brain growth more than the requirements of juvenile ecology.

Reaction norm analysis reveals rapid shifts toward delayed maturation in harvested Lake Erie yellow perch (Perca flavescens).

Harvested marine fish stocks often show a rapid and substantial decline in the age and size at maturation. Such changes can arise from multiple processes including fisheries-induced evolution, phenotypic plasticity, and responses to environmental factors other than harvest. The relative importance of these processes could differ systematically between marine and freshwater systems. We tested for temporal shifts in the mean and within-cohort variability of age- and size-based maturation probabilities of female yellow perch (Perca flavescens Mitchill) from four management units (MUs) in Lake Erie. Lake Erie yellow perch have been commercially harvested for more than a century, and age and size at maturation have varied since sampling began in the 1980s. Our analysis compared probabilistic maturation reaction norms (PMRNs) for cohorts when abundance was lower and harvest higher (1993-1998) to cohorts when abundance was higher and harvest lower (2005-2010). PMRNs have been used in previous studies to detect signs of evolutionary change in response to harvest. Maturation size threshold increased between the early and late cohorts, and the increases were statistically significant for the youngest age in the western MU1 and for older ages in the eastern MU3. Maturation envelope widths, a measure of the variability in maturation among individuals in a cohort, also increased between early and late cohorts in the western MUs where harvest was highest. The highest rates of change in size at maturation for a given age were as large or larger than rates reported for harvested marine fishes where declines in age and size at maturation have been observed. Contrary to the general observation of earlier maturation evolving in harvested stocks, female yellow perch in Lake Erie may be rapidly evolving delayed maturation since harvest was relaxed in the late 1990s, providing a rare example of possible evolutionary recovery.

Intraspecific brain size variation between coexisting sunfish ecotypes.

Variation in spatial complexity and foraging requirements between habitats can impose different cognitive demands on animals that may influence brain size. However, the relationship between ecologically related cognitive performance and brain size is not well established. We test whether variation in relative brain size and brain region size is associated with habitat use within a population of pumpkinseed sunfish composed of different ecotypes that inhabit either the structurally complex shoreline littoral habitat or simpler open-water pelagic habitat. Sunfish using the littoral habitat have on average 8.3% larger brains than those using the pelagic habitat. We found little difference in the proportional sizes of five brain regions between ecotypes. The results suggest that cognitive demands on sunfish may be reduced in the pelagic habitat given no habitat-specific differences in body condition. They also suggest that either a short divergence time or physiological processes may constrain changes to concerted, global modifications of brain size between sunfish ecotypes.

Comparative Analyses of Phenotypic Trait Covariation within and among Populations.

Many morphological, behavioral, physiological, and life-history traits covary across the biological scales of individuals, populations, and species. However, the processes that cause traits to covary also change over these scales, challenging our ability to use patterns of trait covariance to infer process. Trait relationships are also widely assumed to have generic functional relationships with similar evolutionary potentials, and even though many different trait relationships are now identified, there is little appreciation that these may influence trait covariation and evolution in unique ways. We use a trait-performance-fitness framework to classify and organize trait relationships into three general classes, address which ones more likely generate trait covariation among individuals in a population, and review how selection shapes phenotypic covariation. We generate predictions about how trait covariance changes within and among populations as a result of trait relationships and in response to selection and consider how these can be tested with comparative data. Careful comparisons of covariation patterns can narrow the set of hypothesized processes that cause trait covariation when the form of the trait relationship and how it responds to selection yield clear predictions about patterns of trait covariation. We discuss the opportunities and limitations of comparative approaches to evaluate hypotheses about the evolutionary causes and consequences of trait covariation and highlight the importance of evaluating patterns within populations replicated in the same and in different selective environments. Explicit hypotheses about trait relationships are key to generating effective predictions about phenotype and its evolution using covariance data.

Causes and Consequences of Behavioral Interference between Species.

Behavioral interference between species, such as territorial aggression, courtship, and mating, is widespread in animals. While aggressive and reproductive forms of interspecific interference have generally been studied separately, their many parallels and connections warrant a unified conceptual approach. Substantial evidence exists that aggressive and reproductive interference have pervasive effects on species coexistence, range limits, and evolutionary processes, including divergent and convergent forms of character displacement. Alien species invasions and climate change-induced range shifts result in novel interspecific interactions, heightening the importance of predicting the consequences of species interactions, and behavioral interference is a fundamental but neglected part of the equation. Here, we outline priorities for further theoretical and empirical research on the ecological and evolutionary consequences of behavioral interference.

Eco-mechanics of lamellar autotomy in larval damselflies.

In larval damselflies, the self-amputation (autotomy) of the caudal lamellae permits escape from predatory larval dragonflies. Lamellar joint size declines among populations with increasing risk of dragonfly predation, but the breaking force required for autotomy and the biomechanical factors that influence breaking force are unknown. If autotomy enhances survival in larval damselflies, then predation by larval dragonflies should select for joints that require less force to break. We test this adaptive hypothesis by evaluating whether breaking force is negatively related to local predation risk from larval dragonflies. We also test a cuticle structure hypothesis, which predicts that breaking force is positively related to joint size and to joint cuticle thickness because of a structural support relationship between joint and lamella. The peak force necessary for lamellar autotomy was assessed on individual larval Enallagma damselflies collected from populations that varied in risk of predation. Easier lamellar autotomy occurred in larvae from sites with higher predation risk because damselflies from fishless ponds (where predatory larval dragonflies are likely more abundant) had lower breaking forces than those from ponds with fish (where larval dragonfly predation is likely reduced). Furthermore, breaking force was a positive function of joint size and also of total cuticle cross-sectional area after controlling for joint size. This suggests that autotomy may evolve in larval damselflies under selection from small grasping predators such as larval dragonflies by favouring smaller joint size or reduced cuticle area of lamellar joints.

Evolution of growth by genetic accommodation in Icelandic freshwater stickleback.

Classical Darwinian adaptation to a change in environment can ensue when selection favours beneficial genetic variation. How plastic trait responses to new conditions affect this process depends on how plasticity reveals to selection the influence of genotype on phenotype. Genetic accommodation theory predicts that evolutionary rate may sharply increase when a new environment induces plastic responses and selects on sufficient genetic variation in those responses to produce an immediate evolutionary response, but natural examples are rare. In Iceland, marine threespine stickleback that have colonized freshwater habitats have evolved more rapid individual growth. Heritable variation in growth is greater for marine full-siblings reared at low versus high salinity, and genetic variation exists in plastic growth responses to low salinity. In fish from recently founded freshwater populations reared at low salinity, the plastic response was strongly correlated with growth. Plasticity and growth were not correlated in full-siblings reared at high salinity nor in marine fish at either salinity. In well-adapted lake populations, rapid growth evolved jointly with stronger plastic responses to low salinity and the persistence of strong plastic responses indicates that growth is not genetically assimilated. Thus, beneficial plastic growth responses to low salinity have both guided and evolved along with rapid growth as stickleback adapted to freshwater.

Diversifying and correlational selection on behavior toward conspecific and heterospecific competitors in brook stickleback (Culaea inconstans).

Behaviors toward heterospecifics and conspecifics may be correlated because of shared mechanisms of expression in both social contexts (nonadaptive covariation) or because correlational selection favors adaptive covariation. We evaluated these hypotheses by comparing behavior toward conspecifics and heterospecifics in brook stickleback (Culaea inconstans) from three populations sympatric with and three allopatric from a competitor, the ninespine stickleback (Pungitius pungitius). Behavioral traits were classified into three multivariate components: overt aggression, sociability, and activity. The correlation of behavior between social contexts for both overt aggression and activity varied among populations in a way unrelated to sympatry with ninespine stickleback, while mean aggression was reduced in sympatry. Correlations in allopatric populations suggest that overt aggression and activity may genetically covary between social contexts for nonadaptive reasons. Sociability was rarely correlated in allopatry but was consistently correlated in sympatry despite reduced mean sociability, suggesting that correlational selection may favor a sociability syndrome in brook stickleback when they coexist with ninespine stickleback. Thus, interspecific competition may impose diversifying selection on behavior among populations, although the causes of correlated behavior toward conspecifics and heterospecifics and whether it can evolve in one social context independent of the other may depend on the type of behavior.

Contemporary and historical evolutionary processes interact to shape patterns of within-lake phenotypic divergences in polyphenic pumpkinseed sunfish, Lepomis gibbosus.

Historical and contemporary evolutionary processes can both contribute to patterns of phenotypic variation among populations of a species. Recent studies are revealing how interactions between historical and contemporary processes better explain observed patterns of phenotypic divergence than either process alone. Here, we investigate the roles of evolutionary history and adaptation to current environmental conditions in structuring phenotypic variation among polyphenic populations of sunfish inhabiting 12 postglacial lakes in eastern North America. The pumpkinseed sunfish polyphenism includes sympatric ecomorphs specialized for littoral or pelagic lake habitats. First, we use population genetic methods to test the evolutionary independence of within-lake phenotypic divergences of ecomorphs and to describe patterns of genetic structure among lake populations that clustered into three geographical groupings. We then used multivariate analysis of covariance (MANCOVA) to partition body shape variation (quantified with geometric morphometrics) among the effects of evolutionary history (reflecting phenotypic variation among genetic clusters), the shared phenotypic response of all populations to alternate habitats within lakes (reflecting adaptation to contemporary conditions), and unique phenotypic responses to habitats within lakes nested within genetic clusters. All effects had a significant influence on body form, but the effects of history and the interaction between history and contemporary habitat were larger than contemporary processes in structuring phenotypic variation. This highlights how divergence can be better understood against a known backdrop of evolutionary history.

Ecology and evolution of resource-related heterospecific aggression.

Direct interactions among conspecific and heterospecific animals are often mediated by aggressive behavior. We analyze the ecology and evolution of resourc-related heterospecific aggression (HA) by reviewing and meta-analysing 126 studies, contrasting HA with conspecfic aggression (CA), and discussing terminological confusions and conceptual models. HA occurred in 78% of tests (n = 459), suggesting a high prevalence and potential effect on niche use and community structure. The benefits of both CA and HA are linked to resource defensibility and abundance, yet HA can change independently of CA. Ecological inferences about HA are often weak because they assume that interference always results from resource competition, and evolutionary inferences made by comparing HA to CA are also weak because they usually ignore history. We believe that comparisons between situations where a focal species is allopatric from and sympatric with a heterospecfic competitor provide better opportunities to test hypotheses about HA. In general, according to our data set, aggression was higher with increased resource overlap as expected, both because CA was greater than HA, and HA was greater within compared to between genera. Progress in understanding HA requires distinguishing traits (aggressive behavior) from interactions (agonism, interference), as well as from the ecological and evolutionary causer (competition, ancestry) and consequences (dominance, territoriality, exclusion) of those interactions.

Replicated evolution of integrated plastic responses during early adaptive divergence.

Colonization of a novel environment is expected to result in adaptive divergence from the ancestral population when selection favors a new phenotypic optimum. Local adaptation in the new environment occurs through the accumulation and integration of character states that positively affect fitness. The role played by plastic traits in adaptation to a novel environment has generally been ignored, except for variable environments. We propose that if conditions in a relatively stable but novel environment induce phenotypically plastic responses in many traits, and if genetic variation exists in the form of those responses, then selection may initially favor the accumulation and integration of functionally useful plastic responses. Early divergence between ancestral and colonist forms will then occur with respect to their plastic responses across the gradient bounded by ancestral and novel environmental conditions. To test this, we compared the magnitude, integration, and pattern of plastic character responses in external body form induced by shallow versus open water conditions between two sunfish ecomorphs that coexist in four postglacial lakes. The novel sunfish ecomorph is present in the deeper open water habitat, whereas the ancestral ecomorph inhabits the shallow waters along the lake margin. Plastic responses by open water ecomorphs were more correlated than those of their local shallow water ecomorph in two of the populations, whereas equal levels of correlated plastic character responses occurred between ecomorphs in the other two populations. Small but persistent differences occurred between ecomorph pairs in the pattern of their character responses, suggesting a recent divergence. Open water ecomorphs shared some similarities in the covariance among plastic responses to rearing environment. Replication in the form of correlated plastic responses among populations of open water ecomorphs suggests that plastic character states may evolve under selection. Variation between ecomorphs and among lake populations in the covariance of plastic responses suggests the presence of genetic variation in plastic character responses. In three populations, open water ecomorphs also exhibited larger plastic responses to the environmental gradient than the local shallow water ecomorph. This could account for the greater integration of plastic responses in open water ecomorphs in two of the populations. This suggests that the plastic responses of local sunfish ecomorphs can diverge through changes in the magnitude and coordination of plastic responses. Although these results require further investigation, they suggest that early adaptive evolution in a novel environment can include changes to plastic character states. The genetic assimilation of coordinated plastic responses could result in the further, and possibly rapid, divergence of such populations and could also account for the evolution of genes of major effect that contribute to suites of phenotypic differences between divergent populations.