Beren W. Robinson

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 resource-related heterospecific aggression (HA) by reviewing and meta-analyzing 126 studies, contrasting HA with conspecific 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 heterospecific 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 causes (competition, ancestry) and consequences (dominance, territoriality, exclusion) of those interactions.

REPLICATED EVOLUTION OF INTEGRATED PLASTIC RESPONSES DURING EARLY ADAPTIVE DIVERGENCE

Abstract 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.

Foraging performance of diet‐induced morphotypes in pumpkinseed sunfish (Lepomis gibbosus) favours resource polymorphism

Morphological plasticity can influence adaptive divergence when it affects fitness components such as foraging performance. We induced morphological variation in pumpkinseed sunfish (Lepomis gibbosus) ecomorphs and tested for effects on foraging performance. Young‐of‐year pumpkinseed sunfish from littoral and pelagic lake habitats were reared each on a ‘specialist diet’ representing their native habitat‐specific prey, or a ‘generalist diet’ reflecting a combination of native and non‐native prey. Specialist and generalist diets, respectively, induced divergent and intermediate body forms. Specialists had the highest capture success on their native prey whereas generalist forms were inferior. Specialists faced trade‐offs across prey types. However, pelagic specialists also had the highest intake rate on both prey types suggesting that foraging trade‐offs are relaxed when prey are abundant. This increases the likelihood of a resource polymorphism because the specialized pelagic form can be favoured by directional selection when prey are abundant and by diversifying selection when prey resources are restricted.

HETEROSPECIFIC AGGRESSION AND ADAPTIVE DIVERGENCE IN BROOK STICKLEBACK (CULAEA INCONSTANS)

Abstract Agonistic behavior between heterospecifics, in which individuals of one species attack another, may cause a subordinate species to shift resource or habitat use. Subsequent evolutionary responses to selection may mimic shifts expected under ecological character displacement, but with no role played by exploitative competition. Alternatively, aggressive behavior can evolve when fitness is improved by excluding members of a coexisting species from a defendable resource through interference. We tested whether heterospecific agonistic behavior has evolved in brook stickleback (Culaea inconstans) by comparing replicate allopatric populations to those sympatric with ninespine stickleback (Pungitius pungitius). We also tested for heritable variation in heterospecific aggressive behavior by rearing family groups in a common environment. Allopatric populations of brook stickleback were more aggressive than ninespine stickleback, suggesting that pre-existing aggression in brook stickleback contributed to niche shifts by ninespine stickleback. In addition, sympatric adult brook stickleback were more aggressive toward ninespine stickleback than brook stickleback from allopatric populations. Overt heterospecific aggressive behaviors were heritable, and aggression in juvenile brook stickleback increased with age in sympatric but not in allopatric populations reared in a common environment. Brook stickleback have evolved increased aggression when they coexist with ninespine stickleback. These stickleback communities have been structured by both evolved and pre-existing variation in heterospecific aggressive behavior in brook stickleback.

Testing alternative explanations of character shifts against ecological character displacement in brook sticklebacks (Culaea inconstans) that coexist with ninespine sticklebacks (Pungitius pungitius)

Ecological character displacement (ECD) provides opportunities to test how resource competition generates diversifying selection that results in adaptive divergence. We quantify an association between phenotypic and ecological divergence between two similar small fishes, brook (Culaea inconstans) and ninespine (Pungitius pungitius) sticklebacks, in replicate northern Ontario lakes, Canada. The two species partition resources and habitat, where they coexist, and brooks that coexist with ninespines are more benthically specialized in body form and diet than brooks from local allopatric populations. Here we test various explanations for this pattern. Chance is unlikely to have been the primary cause because divergence is replicated in three separate populations. Preliminary comparisons indicate that resource availability and a variety of abiotic ecological conditions are generally similar between sympatric and allopatric sites, and so do not readily account for the divergence. Biased colonization or extinction is less likely to account for the divergence because character values in sympatry tend to exceed those in allopatry, as expected if they have repeatedly evolved under diversifying selection. Recent studies have also demonstrated that these two species compete, and that competitive effects are more severe for allopatric compared to sympatric brook forms, as predicted if divergence reflects the ghost of competition past. Ongoing studies indicate heritable variation in this system. Our results suggest that even small amounts of character shifts can influence competition and hence relative fitness, further implicating a role for ECD in the evolution of biodiversity.

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.

Analyzing nested variation in the body form of Lepomid sunfishes

Phylogenetic hierarchies are often composed of younger diverging lineages nested within older diverging lineages. Comparing phenotypic variation among several hierarchical levels can be used to test hypotheses about selection, phenotypic evolution and speciation. Such hierarchical comparisons have only been performed in threespine stickleback, and so here we use a hierarchical pattern of divergences between near-shore littoral and off-shore pelagic habitats to test for selection on the evolution of body form in Lepomis sunfish in lakes. We compare variation in external body form between fish from littoral and pelagic habitats at three levels: among ecomorphs within individual lake populations (intrapopulation), among populations of the same species in different lakes (interpopulation), and between bluegill and pumpkinseed sunfish species (interspecifically). Using geometric morphometric methods, we first demonstrate that interpopulation variation in mean body form of pumpkinseed sunfish varies with the presence of pelagic habitat. We then incorporate these results with existing data in order to test the similarity of phenotypic divergence between littoral and pelagic habitats at different hierarchical levels. Parallel relationships between certain body form traits (head length, caudal length and pectoral length) and habitat occur at all three levels suggesting that selection persistently acts at all levels to diversify these traits and so may contribute to species formation. For other traits (caudal depth and pectoral altitude), divergence between habitats is inconsistent at different hierarchical levels. Thus, nested biological variation in Lepomid body form reflects a history of deterministic selection and historical contingency, and also identifies traits that likely have likely influenced fitness and so serve important functions.

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.

A New Statistical Test of Fitness Set Data from Reciprocal Transplant Experiments Involving Intermediate Phenotypes

Experimental biologists use reciprocal transplant experiments (RTEs) involving divergent forms to test hypotheses about fitness trade‐offs across, and local adaptation to, native environments. Additional evolutionary hypotheses about diversifying selection, the evolution of specialization, and the coexistence of specialists and generalists are only testable when the RTE also includes intermediate (or alternatively generalist) forms. Environmental variation makes such RTEs challenging, and so strategies that increase their effectiveness are useful. Here, we focus on improvements to the efficiency of RTEs involving intermediate forms with respect to the experimental design and the analysis of the resulting data. We provide a likelihood ratio–based test that offers increased statistical power and robustness relative to another test involving nonlinear regression, when used both for simulated data sets and for data from a study of two divergent fish species and their hybrids transplanted between two lake habitats. The test can be used with unequal numbers of observations, unequal variances, and binomial‐type survival data and other nonnormal data. Simulations suggest that having equal numbers of experimental units in each phenotype‐environment combination is reasonable. The intentional pairing of observations between environmental conditions (by using clones, full sibs, or half‐sibs) is beneficial when paired observations have fitnesses that are negatively related between conditions but is detrimental with positive relatedness. Our methods can be extended to study more than two divergent forms.

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.