Discrete foraging niches promote ecological, phenotypic, and genetic divergence in sympatric whitefish (Coregonus lavaretus)

Natural populations often vary in their degree of ecological, morphological and genetic divergence. This variation can be arranged along an ecological speciation continuum of increasingly discrete variation, with high inter-individual variation at one end and well defined species in the other. In postglacial fishes, evolutionary divergence has commonly resulted in the co-occurrence of a pelagic and a benthic specialist. We studied three replicate lakes supporting sympatric pelagic and benthic European whitefish (Coregonus lavaretus (L.)) morphs in search for early signs of possible further divergence into more specialized niches. Using stomach content data (recent diet) and stable isotope analyses (time-integrated measure of trophic niche use), we observed a split in the trophic niche within the benthic whitefish morph, with individuals specializing on either littoral or profundal resources. This divergence in resource use was accompanied by small but significant differences in an adaptive morphological trait (gill raker number) and significant genetic differences between fish exploiting littoral and profundal habitats and foraging resources. The same pattern of parallel divergence was found in all three lakes, suggesting similar natural selection pressures driving and/or maintaining the divergence. The two levels of divergence (a clear and robust benthic – pelagic and a more subtle littoral – profundal divergence) observed in this study apparently represent different stages in the process of ecological speciation.     

Genetic divergence in morphology-performance mapping between Misty Lake and inlet stickleback

Different environments should select for different aspects of organismal performance, which should lead to correlated divergence in morphological traits that influence performance. The result should be genetic divergence in aspects of performance, morphology and associations ('maps') between morphology and performance. Testing this hypothesis requires quantifying performance and morphology in multiple populations after controlling for environmental differences, but this is rarely attempted. We used a common-garden experiment to examine morphology and several aspects of swimming performance within and between the lake and inlet populations of threespine stickleback (Gasterosteus aculeatus) from the Misty system, Vancouver Island, Canada. Controlling for body size, lake stickleback had shallower bodies, larger caudal fins and smaller pelvic girdles. With or without morphological covariates, lake stickleback showed greater performance in both sustained and burst swimming. In contrast, inlet stickleback showed greater manoeuverability than did lake stickleback in some analyses. Morphology-performance relationships were decoupled when considering variation within vs. between populations. Moreover, morphology-performance mapping differed between the two populations. Based on these observations, we advance a hypothesis for why populations adapting to different environments should show adaptive genetic divergence in morphology-performance mapping.     

The interaction of resource use and gene flow on the phenotypic divergence of benthic and pelagic morphs of Icelandic Arctic charr (Salvelinus alpinus)

Conceptual models of adaptive divergence and ecological speciation in sympatry predict differential resource use, phenotype–environment correlations, and reduced gene flow among diverging phenotypes. While these predictions have been assessed in past studies, connections among them have rarely been assessed collectively. We examined relationships among phenotypic, ecological, and genetic variation in Arctic charr (Salvelinus alpinus) from six Icelandic localities that have undergone varying degrees of divergence into sympatric benthic and pelagic morphs. We characterized morphological variation with geometric morphometrics, tested for differential resource use between morphs using stable isotopes, and inferred the amount of gene flow from single nucleotide polymorphisms. Analysis of stable isotopic signatures indicated that sympatric morphs showed similar difference in resource use across populations, likely arising from the common utilization of niche space within each population. Carbon isotopic signature was also a significant predictor of individual variation in body shape and size, suggesting that variation in benthic and pelagic resource use is associated with phenotypic variation. The estimated percentage of hybrids between sympatric morphs varied across populations (from 0% to 15.6%) but the majority of fish had genotypes (ancestry coefficients) characteristic of pure morphs. Despite evidence of reduced gene flow between sympatric morphs, we did not detect the expected negative relationship between divergence in resource use and gene flow. Three lakes showed the expected pattern, but morphs in the fourth showed no detectable hybridization and had relatively low differences in resource use between them. This coupled with the finding that resource use and genetic differentiation had differential effects on body shape variation across populations suggests that reproductive isolation maintains phenotypic divergence between benthic and pelagic morphs when the effects of resource use are relatively low. Our ability to assess relationships between phenotype, ecology, and genetics deepens our understanding of the processes underlying adaptive divergence in sympatry.     

Genetic and morphological divergence along the littoral–pelagic axis in two common and sympatric fishes: perch,Perca fluviatilis (Percidae) and roach,Rutilus rutilus (Cyprinidae)

Individuals are constantly in competition with one another and, on both ecological and evolutionary timescales, processes act to reduce this competition and promote the gain of fitness advantages via diversification. Here we have investigated the genetic (AFLP) and morphological (geometric morphometrics) aspects of the littoral–pelagic axis, a commonly observed resource polymorphism in freshwater fishes of postglacial lakes. We found a large degree of variation in the genetic and morphological divergence between littoral and pelagic perch and roach across Swedish lakes. Although there was evidence of assortative mating (elevated kinship values) in both species, we could not find any significant coupling of morphology and genetic divergence. Instead, there was evidence that the extent of resource polymorphism may be largely caused by phenotypic plasticity. These results suggest that assortative mating, which can lead to genetically determined adaptive divergence, does occur in these species, particularly perch, but not according to genetically fixed morphological traits. The behavioural mechanisms facilitating associative mating need to be investigated to explore the interaction between phenotypic plasticity and adaptive genetic divergence and their roles in diversification. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 929–940.     

Phenotypic plasticity, heterochrony and ontogenetic repatterning during juvenile development of divergent Arctic charr (Salvelinus alpinus)

Phenotypic plasticity is a developmental process that plays a role as a source of variation for evolution. Models of adaptive divergence make the prediction that increasing ecological specialization should be associated with lower levels of plasticity. We tested for differences in the magnitude, rate and trajectory of morphological plasticity in two lake populations of Arctic charr (Salvelinus alpinus) that exhibited variation in the degree of resource polymorphism. We reared offspring on diet treatments that mimicked benthic and pelagic prey. Offspring from the more divergent population had lower levels of morphological plasticity. Allometry influenced the rate of shape change over ontogeny, with differences in rate among ecomorphs being minimal when allometric variation was removed. However, plasticity in the spatial trajectory of development was extensive across ecomorphs, both with and without the inclusion of allometric variation, suggesting that different aspects of shape development can evolve independently.     

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.     

Parallels,nonparallels, and plasticity in population differentiation of threespine stickleback within a lake

The frequent occurrence of parallel phenotypic divergence in similar habitats is often evoked when emphasizing the role of ecology in adaptive radiation and speciation. However, because phenotypic plasticity can contribute to the observed pattern of divergence, confirmation of divergence at loci underlying phenotypic traits is important for confirming adaptive divergence. In the present study, we examine parallel morphological, neutral, and potentially adaptive genetic divergence of threespine stickleback inhabiting different habitats within a lake. Three genetic clusters best explained the neutral genetic structure within the lake; however, morphological differences were only weakly connected to genetic clusters and there was considerable phenotypic variation within clusters. Among the factors that could contribute to the observed pattern of morphological and genetic divergence are phenotypic plasticity, selective mortality of hybrids, and habitat choice based on morphology. Several loci are identified as outliers indicating divergent selection between the morphs and some parallels in morphological and adaptive genetic divergence are found in stickleback spawning at two lava sites. However, neutral genetic structure indicates considerable genetic connectivity among the two lava sites, and the parallels in morphology may therefore represent selective distribution of phenotypes rather than parallel divergence. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98 , 803–813.     

Colour plasticity and background matching in a threespine stickleback species pair

Examining differences in colour plasticity between closely‐related species in relation to the heterogeneity of background colours found in their respective habitats may offer important insight into how cryptic colour change evolves in natural populations. In the present study, we examined whether nonbreeding dorsal body coloration has diverged between sympatric species of stickleback along with changes in habitat‐specific background colours. The small, limnetic species primarily occupies the pelagic zone and the large, benthic species inhabits the littoral zone. We placed benthic and limnetic sticklebacks against extremes of habitat background colours and measured their degree of background matching and colour plasticity. Benthics matched the littoral background colour more closely than did the limnetics, although there was no difference between species in their resemblance to the pelagic background colour. Benthics were able to resemble both background colours by exhibiting greater directional colour plasticity in their dorsal body coloration than limnetics, which may be an adaptive response to the greater spectral heterogeneity of the littoral zone. The present study highlights how habitat‐specific spectral characteristics may shape cryptic coloration differences between stickleback species. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 902–914.     

Ecological speciation in postglacial European whitefish: rapid adaptive radiations into the littoral,pelagic, and profundal lake habitats

Understanding how a monophyletic lineage of a species diverges into several adaptive forms has received increased attention in recent years, but the underlying mechanisms in this process are still under debate. Postglacial fishes are excellent model organisms for exploring this process, especially the initial stages of ecological speciation, as postglacial lakes represent replicated discrete environments with variation in available niches. Here, we combine data of niche utilization, trophic morphology, and 17 microsatellite loci to investigate the diversification process of three sympatric European whitefish morphs from three northern Fennoscandian lakes. The morphological divergence in the gill raker number among the whitefish morphs was related to the utilization of different trophic niches and was associated with reproductive isolation within and across lakes. The intralacustrine comparison of whitefish morphs showed that these systems represent two levels of adaptive divergence: (1) a consistent littoral–pelagic resource axis; and (2) a more variable littoral–profundal resource axis. The results also indicate that the profundal whitefish morph has diverged repeatedly from the ancestral littoral whitefish morph in sympatry in two different watercourses. In contrast, all the analyses performed revealed clustering of the pelagic whitefish morphs across lakes suggesting parallel postglacial immigration with the littoral whitefish morph into each lake. Finally, the analyses strongly suggested that the trophic adaptive trait, number of gill rakers, was under diversifying selection in the different whitefish morphs. Together, the results support a complex evolutionary scenario where ecological speciation acts, but where both allopatric (colonization history) and sympatric (within watercourse divergence) processes are involved.     

Critical swimming velocities of juvenile sockeye salmon and kokanee, the anadromous and non-anadromous forms of Oncorhynchus nerka (Walbaum)

In streams tributary to the North Pacific, anadromous sockeye salmon and non-anadromous kokanee, Oncorhynchus nerka (Walbaum), occasionally spawn sympatrically and male kokanee may act as 'sneaks’to spawn with the larger female sockeye. Despite this interbreeding, sockeye and kokanee exhibit persistent biochemical genetic differences at several enzyme loci. Genetic differences between forms may be maintained by selection against‘hybrids’due to the different life histories of sockeye and kokanee; sockeye make extensive smolt, oceanic, and spawning migrations while kokanee reside permanently in fresh water. We tested the sustained swimming abilities of juvenile sockeye, kokanee, and sockeye (female) × kokanee (male) hybrids to see if hybrids were inferior to sockeye in a trait that is probably under stronger selection in an anadromous life history. Sockeye had significantly greater mean critical swimming velocities (U_crit) than kokanee of the same size raised under identical conditions (8.3 v. 7.3 body lengths s^?1 respectively). When tested 1 month later the mean U_crit of sockeye was only marginally greater than that for sockeye × kokanee hybrids (both c. 6.6 body lengths s^?1). Sockeye swimming performance was also less variable than that of either kokanee or hybrids. Sockeye tended to have slimmer bodies and longer caudal regions than kokanee or sockeye × kokanee hybrids of the same size. Sockeye also had significantly more vertebrae than kokanee and hybrids, while hybrids had more vertebrae than kokanee. These morphological differences may have contributed to the differences in swimming performance. We concluded: (i) that juvenile sockeye and kokanee have diverged with respect to sustained swimming performance and that reduced performance by kokanee may be due to relaxed selection for sustained swimming performance associated with their non-anadromous life history, (ii) that sockeye × kokanee hybrids appear to have modestly lower swimming capabilities than pure sockeye, and (iii) if the variability in swimming performance is associated with differences in survival in nature, then such differences may promote divergence between sympatric sockeye and kokanee.     

Trophic polymorphism in introduced pumpkinseed (<Emphasis Type="Italic">Lepomis gibbosus</Emphasis>) inhabiting Iberian reservoirs

Introduced pumpkinseed in Iberian reservoirs display marked external morphological differentiation along two simultaneous dimensions of flow and trophic structure. We assessed the degree of internal morphological differentiation using gill rakers, pharyngeal jaws and the levator posterior muscle among pumpkinseeds occupying four different habitats and determined whether prey consumption accounted for any discernible differences in feeding structures among ecomorphs. Results showed significant differentiation by habitat based on pharyngeal muscle and jaw dimensions in all study reservoirs, with pelagic pumpkinseeds having smaller jaws than littoral pumpkinseeds in four of the five reservoirs. Gill rakers, however, differentiated morphs in only three of the five reservoirs, corresponding to differences in zooplankton consumption among pelagic and littoral individuals in those reservoirs. Based on all internal morphological traits, greater divergence was seen along the littoral-pelagic trophic axis in the lacustrine zones of reservoirs compared to the fluvial zone. Overall differences noted in internal morphology are likely the result of phenotypic plasticity; the ability of this species to readily adapt to changing physical environments may explain the success of the pumpkinseed in its introduced range.     

Assessing the ecological relevance of swimming performance traits: a case study of bluegill sunfish (<Emphasis Type="Italic">Lepomis macrochirus</Emphasis>)

A variety of fish species show habitat-related variation in traits associated with swimming performance and foraging behavior. This commonly manifests as a distinction between open water and shallow water littoral ecotypes. In bluegill sunfish (Lepomis macrochirus), open water fish exhibit greater energy economy and speed during sustained locomotion than those from the littoral, whereas littoral fish were more maneuverable than their open water counterparts. These distinctions are associated with variation in diet and foraging behavior and may represent a resource polyphenism that enhances fitness through more effective exploitation of particular habitat types. A lack of field data means that polyphenisms have not been placed in context with swimming behavior in the field. We have used 3D videography to quantify bluegill field swimming performance in open water and littoral habitats. This revealed patterns of performance variation that parallel the trait variation previously established in the laboratory. Open water fish utilized faster average swimming speeds than inshore fish, while indicators of nonlinearity and unsteadiness were greater in the littoral fish. There are, however, differences in propulsive behavior between the field and laboratory. Pectoral-fin-powered, median-paired fin swimming is rarely employed by open water fish. Field body-caudal fin swimming involves short sequences of propulsive tail beats interspersed with gliding, rather than the repeated propulsive cycles employed under steady-state conditions. This suggests a need to re-evaluate the applicability of steady-state performance traits to behavior and fitness in the field and highlights the general importance of obtaining field performance data.     

STRONG ASSORTATIVE MATING BY DIET,COLOR, SIZE,AND MORPHOLOGY BUT LIMITED PROGRESS TOWARD SYMPATRIC SPECIATION IN A CLASSIC EXAMPLE: CAMEROON CRATER LAKE CICHLIDS

Models predict that sympatric speciation depends on restrictive parameter ranges, such as sufficiently strong disruptive selection and assortative mating, but compelling examples in nature have rarely been used to test these predictions. I measured the strength of assortative mating within a species complex of Tilapia in Lake Ejagham, Cameroon, a celebrated example of incipient sympatric adaptive radiation. This species complex is in the earliest stages of speciation: morphological and ecological divergence are incomplete, species differ primarily in breeding coloration, and introgression is common. I captured 27 mated pairs in situ and measured the diet, color, size, and morphology of each individual. I found strong assortative mating by color, size, head depth, and dietary source of benthic or pelagic prey along two independent dimensions of assortment. Thus, Ejagham Tilapia showed strong assortative mating most conducive to sympatric speciation. Nonetheless, in contrast to a morphologically bimodal Sarotherodon cichlid species pair in the lake, Ejagham Tilapia show more limited progress toward speciation, likely due to insufficient strength of disruptive selection on morphology estimated in a previous study (γ = 0.16). This supports the predicted dependence of sympatric speciation on strong assortment and strong disruptive selection by examining a potentially stalled example in nature.     

The influence of swimming demand on phenotypic plasticity and morphological integration: a comparison of two polymorphic charr species

In northern freshwater lakes, several fish species have populations composed of discrete morphs, usually involving a divergence between benthic and limnetic morphs. Although it has been suggested that swimming demand plays an important role in morphological differentiation, thus influencing habitat selection, it is unclear how it affects reaction norms, patterns in character correlation, and levels of morphological integration. We examined whether swimming demand could induce morphological plasticity in the directions expected under divergent habitat selection, and evaluated its influence on the morphological integration in Arctic charr (Salvelinus alpinus) and brook charr (S. fontinalis), two congeneric species exhibiting conspicuous and subtle resource polymorphism, respectively. We found that changes in morphology were induced by differential swimming demands in both species. The length of the pectoral fin was the character that responded most strongly according to the predicted morphological expectations under divergent habitat selection. High levels of morphological plasticity, relatively low levels of integration, and differences found in the morphological correlation structure among water velocity treatments suggest that constraints on morphological change are unlikely in either species, thus allowing great potential for phenotypic flexibility in both species. The magnitude of character integration, however, was larger for Arctic charr than for brook charr. This latter result is discussed in the light of the differences in the level of polymorphism between the two species in the wild. The results of the present study indicate that swimming demand alone may not be sufficient to generate the polymorphism encountered in nature. Given that both diet and swimming demands can induce morphological changes, it would be important to conduct experiments targeting the interaction between the morphological modules related to trophic and swimming demands.     

Comparing the consequences of natural selection,adaptive phenotypic plasticity,and matching habitat choice for phenotype–environment matching,population genetic structure,and reproductive isolation in meta‐populations

Organisms commonly experience significant spatiotemporal variation in their environments. In response to such heterogeneity, different mechanisms may act that enhance ecological performance locally. However, depending on the nature of the mechanism involved, the consequences for populations may differ greatly. Building on a previous model that investigated the conditions under which different adaptive mechanisms (co)evolve, this study compares the ecological and evolutionary population consequences of three very different responses to environmental heterogeneity: matching habitat choice (directed gene flow), adaptive plasticity (associated with random gene flow), and divergent natural selection. Using individual‐based simulations, we show that matching habitat choice can have a greater adaptive potential than plasticity or natural selection: it allows for local adaptation while protecting genetic polymorphism despite global mating or strong environmental changes. Our simulations further reveal that increasing environmental fluctuations and unpredictability generally favor the emergence of specialist genotypes but that matching habitat choice is better at preventing local maladaptation by individuals. This confirms that matching habitat choice can speed up the genetic divergence among populations, cause indirect assortative mating via spatial clustering, and hence even facilitate sympatric speciation. This study highlights the potential importance of directed dispersal in local adaptation and speciation, stresses the difficulty of deriving its operation from nonexperimental observational data alone, and helps define a set of ecological conditions which should favor its emergence and subsequent detection in nature.     

Niche specialization influences adaptive phenotypic plasticity in the threespine stickleback

Phenotypic plasticity may be favored in generalist populations if it increases niche width, even in temporally constant environments. Phenotypic plasticity can increase the frequency of extreme phenotypes in a population and thus allow it to make use of a wide resource spectrum. Here we test the prediction that generalist populations should be more plastic than specialists. In a common-garden experiment, we show that solitary, generalist populations of threespine sticklebacks inhabiting small coastal lakes of British Columbia have a higher degree of morphological plasticity than the more specialized sympatric limnetic and benthic species. The ancestral marine stickleback showed low levels of plasticity similar to those of sympatric sticklebacks, implying that the greater plasticity of the generalist population has evolved recently. Measurements of wild populations show that those with mean trait values intermediate between the benthic and limnetic values indeed have higher morphological variation. Our data indicate that plasticity can evolve rapidly after colonization of a new environment in response to changing niche use.     

Juvenile divergence in adaptive traits among seven sympatric fish ecomorphs arises before moving to different lacustrine habitats

Identifying the mechanisms initiating sympatric diversification in vertebrates has remained a conceptual challenge. Here, we analyse an assemblage of sympatric charr (Salvelinus malma) morphs from landlocked Lake Kronotskoe basin as a model to uncover the divergence pathways in freshwater fishes during the early life history stages. All morphs have distinct developmental biology, but a similar developmental rate retardation compared to the ancestor. Our study reveals that adult morphological differences, which acquire functionality at maturation, originate in the early juvenile stages due to heterochrony in skeletogenesis and allometric changes triggered by variation in metabolic activity. The craniofacial differences among the morphs result from asynchronous development of several skeletal modules. The accelerated ossification of teeth‐armed bones occurs in predatory feeding morphs, whereas cranial cover ossification is promoted in benthivorous morphs. These contrasting growth patterns have led to seven phenotypes that span a range far beyond the ancestral variability. The most distinct morphs are a riverine spawning, epilimnetic predator and a lacustrine spawning, profundal benthic feeder. Taken together, we argue that the adaptive morphological differentiation in these sympatric freshwater fishes is driven by diverging patterns in ossification rate and metabolic activity against a background of uneven somatic growth. This divergence is primarily associated with basic environmental differences on the nursery grounds that might be unrelated to resource use. This nonheritable phenotype divergence is then exposed to natural selection that could result in further adaptive genetic changes.     

Constraints on adaptive evolution: the functional trade-off between reproduction and fast-start swimming performance in the Trinidadian guppy (Poecilia reticulata)

The empirical study of natural selection reveals that adaptations often involve trade-offs between competing functions. Because natural selection acts on whole organisms rather than isolated traits, adaptive evolution may be constrained by the interaction between traits that are functionally integrated. Yet, few attempts have been made to characterize how and when such constraints are manifested or whether they limit the adaptive divergence of populations. Here we examine the consequences of adaptive life-history evolution on locomotor performance in the live-bearing guppy. In response to increased predation from piscivorous fish, Trinidadian guppies evolve an increased allocation of resources toward reproduction. These populations are also under strong selection for rapid fast-start swimming performance to evade predators. Because embryo development increases a female's wet mass as she approaches parturition, an increased investment in reproductive allocation should impede fast-start performance. We find evidence for adaptive but constrained evolution of fast-start swimming performance in laboratory trials conducted on second-generation lab-reared fish. Female guppies from high-predation localities attain a faster acceleration and velocity and travel a greater distance during fast-start swimming trials. However, velocity and distance traveled decline more rapidly over the course of pregnancy in these same females, thus reducing the magnitude of divergence in swimming performance between high- and low-predation populations. This functional trade-off between reproduction and swimming performance reveals how different aspects of the phenotype are integrated and highlights the complexity of adaptation at the whole-organism level.     

Do assemblages of Coregonus (Teleostei: Salmoniformes) in the Central Alpine region of Europe represent species flocks?

To examine models of evolution for Coregonus from the Central Alpine region of Europe, 20 populations from nine lakes were assessed for variation at six microsatellite DNA loci. Patterns of variation were tested against three evolutionary models: phenotypic plasticity, multiple invasions of lakes by divergent forms, and within-lake radiation of species flocks. All sympatric and all but one allopatric pairs of populations were significantly divergent in allele frequencies. Pairwise F -statistics indicated reduced gene flow among phenotypically divergent sympatric populations. These results reject the hypothesis that within-lake morphological and ecological diversity reflects phenotypic plasticity within a single gene pool. Genetic similarity was higher among forms within lakes than between populations of the same form in different lakes. Among-lake divergence was primarily a product of allele size differences. Mantel tests contrasting patterns of genetic divergence against patterns predicted from the multiple invasions and species flocks models indicated that the latter is the best explanation of the observed genetic variation. Thus, reproductively isolated species diverged within lakes, with similar patterns repeatedly emerging among lakes. While this study argues for a particular mode of evolution in Central Alpine Coregonus , the taxonomy of these forms remains unresolved.