Sympatric Divergence and Performance Trade-Offs of Bluegill Ecomorphs

Phenotypic plasticity in response to environmental cues can create distinct morphological types within populations. This variation in form, and potentially function, may be a factor in initiating population divergence and the formation of new species. Here we show the translation of sympatric, habitat-specific morphological divergence into performance differences in energy economy, maneuverability and steady-state locomotion. Littoral and pelagic bluegill sunfish ecomorphs show differences in performance that appear adaptive within their respective habitats: greater maneuverability in the heavily vegetated littoral; greater steady-state swimming speed and economy in the open-water pelagic. This represents a trade-off in unsteady versus steady swimming performance, likely because morphological features associated with maximizing maneuverability are incompatible with enhancing steady-swimming performance. This may constrain the direction of adaptive change, maintaining the divergence created by phenotypic plasticity. The combination of habitat specific sympatric adaptation and constraints imposed by performance trade-offs may be an important factor underlying the high rate of speciation in freshwater fishes from post-glacial lakes.     

Convergent evolutionary processes driven by foraging opportunity in two sympatric morph pairs of Arctic charr with contrasting post‐glacial origins

The expression of two or more discrete phenotypes amongst individuals within a species (morphs) provides multiple modes upon which selection can act semi‐independently, and thus may be an important stage in speciation. In the present study, we compared two sympatric morph systems aiming to address hypotheses related to their evolutionary origin. Arctic charr in sympatry in Loch Tay, Scotland, exhibit one of two discrete, alternative body size phenotypes at maturity (large or small body size). Arctic charr in Loch Awe segregate into two temporally segregated spawning groups (breeding in either spring or autumn). Mitochondrial DNA restriction fragment length polymorphism analysis showed that the morph pairs in both lakes comprise separate gene pools, although segregation of the Loch Awe morphs is more subtle than that of Loch Tay. We conclude that the Loch Awe morphs diverged in situ (within the lake), whereas Loch Tay morphs most likely arose through multiple invasions by different ancestral groups that segregated before post‐glacial invasion (i.e. in allopatry). Both morph pairs showed clear trophic segregation between planktonic and benthic resources (measured by stable isotope analysis) but this was significantly less distinct in Loch Tay than in Loch Awe. By contrast, both inter‐morph morphological and life‐history differences were more subtle in Loch Awe than in Loch Tay. The strong ecological but relatively weak morphological and life‐history divergence of the in situ derived morphs compared to morphs with allopatric origins indicates a strong link between early ecological and subsequent genetic divergence of sympatric origin emerging species pairs. The emergence of parallel specialisms despite distinct genetic origins of these morph pairs suggests that the effect of available foraging opportunities may be at least as important as genetic origin in structuring sympatric divergence in post‐glacial fishes with high levels of phenotypic plasticity. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

Recent speciation between sympatric Tanganyikan cichlid colour morphs

Lake Tanganyika, Africa's oldest lake, harbours an impressive diversity of cichlid fishes. Although diversification in its radiating groups is thought to have been initially rapid, cichlids from Lake Tanganyika show little evidence for ongoing speciation. In contrast, examples of recent divergence among sympatric colour morphs are well known in haplochromine cichlids from Lakes Malawi and Victoria. Here, we report genetic evidence for recent divergence between two sympatric Tanganyikan cichlid colour morphs. These Petrochromis morphs share mitochondrial haplotypes, yet microsatellite loci reveal that their sympatric populations form distinct genetic groups. Nuclear divergence between the two morphs is equivalent to that which arises geographically within one of the morphs over short distances and is substantially smaller than that among other sympatric species in this genus. These patterns suggest that these morphs diverged only recently, yet that barriers to gene flow exist which prevent extensive admixture despite their sympatric distribution. The morphs studied here provide an unusual example of active diversification in Lake Tanganyika's generally ancient cichlid fauna and enable comparisons of speciation processes between Lake Tanganyika and other African lakes.     

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.     

Genetic divergence among sympatric colour morphs of the Dalmatian wall lizard (<Emphasis Type="Italic">Podarcis melisellensis</Emphasis>)

If alternative phenotypes in polymorphic populations do not mate randomly, they can be used as model systems to study adaptive diversification and possibly the early stages of sympatric speciation. In this case, non random mating is expected to support genetic divergence among the different phenotypes. In the present study, we use population genetic analyses to test putatively neutral genetic divergence (of microsatellite loci) among three colour morphs of the lizard Podarcis melisellensis, which is associated with differences in male morphology, performance and behaviour. We found weak evidence of genetic divergence, indicating that gene flow is somewhat restricted among morphs and suggesting possible adaptive diversification.     

Morphological divergence and origin of sympatric populations of European whitefish (Coregonus lavaretus L.) in Lake Femund, Norway

Combining morphological and genetic analysis, we compared patterns of diversification within and between morphs among sympatric European whitefish (Coregonus lavaretus L.) populations in Lake Femund, Norway. Seven external populations, from potential colonization routes into Lake Femund were included. We found that deep-, shallow-, river- and bay spawning populations are distinct morphs in Lake Femund. Within morphs, populations range from being similar genetically (Fst=0-0.005) among deep-spawning populations to being highly differentiated (Fst=0.153) between bay-spawning populations. Between morphs, genetic differences ranged from a low (Fst=0.008-0.022) between deep- and shallow-spawning populations to high difference (Fst=0.125-0.143) between shallow- and bay-spawning populations. A higher proportion of molecular variance was seen among (3.9%) than within morphs (2.8%). The adaptive gene combinations behind the four morphs seem to have originated within the lake, although the lake could have been colonized from more than one source population.     

Rugged adaptive landscapes shape a complex,sympatric radiation

Strong disruptive ecological selection can initiate speciation, even in the absence of physical isolation of diverging populations. Species evolving under disruptive ecological selection are expected to be ecologically distinct but, at least initially, genetically weakly differentiated. Strong selection and the associated fitness advantages of narrowly adapted individuals, coupled with assortative mating, are predicted to overcome the homogenizing effects of gene flow. Theoretical plausibility is, however, contrasted by limited evidence for the existence of rugged adaptive landscapes in nature. We found evidence for multiple, disruptive ecological selection regimes that have promoted divergence in the sympatric, incipient radiation of ‘sharpfin’ sailfin silverside fishes in ancient Lake Matano (Sulawesi, Indonesia). Various modes of ecological specialization have led to adaptive morphological differences between the species, and differently adapted morphs display significant but incomplete reproductive isolation. Individual fitness and variation in morphological key characters show that disruptive selection shapes a rugged adaptive landscape in this small but complex incipient lake fish radiation.     

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.     

Basic description and some notes on the evolution of seven sympatric morphs of Dolly Varden Salvelinus malma from the Lake Kronotskoe Basin

The study examines the basic morphological and ecological features of Dolly Varden from Lake Kronotskoe (Russia, Kamchatka). Seven valid morphs different in head proportions, feeding, timing, and place of spawning have been determined in this ecosystem. The basic morphometric characteristics clearly separate Lake Kronotskoe morphs from each other, as well as from its potential ancestor (Dolly Varden). According to CVA analysis, the most notable morphological characteristics determining the mouth position are the length of a lower jaw and rostrum. Furthermore, five of seven morphs inhabit different depth zones of the lake and feed on different food resources. Our data suggest that reproductive isolation may be maintained by temporal/spatial isolation for two morphs with lacustrine spawning, and by spatial isolation only for the rest of the morphs with riverine spawning. The sympatric diversity of the Lake Kronotskoe charrs is exceptionally wide, and there are no other examples for seven sympatric morphs of genus Salvelinus to coexist within a single ecosystem. This study puts forward a three‐step hypothetical model of charr divergence in Lake Kronotskoe as a potential ground for future studies.     

Bone calcification rate as a factor of craniofacial transformations in salmonid fish: Insights from an experiment with hormonal treatment of calcium metabolism

Adaptation to different environments can be achieved by physiological shifts throughout development. Hormonal regulators shape the physiological and morphological traits of the evolving animals making them fit for the particular ecological surroundings. We hypothesized that the artificially induced hypersynthesis of calcitonin and parathyroid hormone mutually influencing calcium metabolism could affect bone formation during early ontogeny in fish imitating the heterochrony in craniofacial ossification in natural adaptive morphs. Conducting an experiment, we found that the long-standing treatment of salmonid juveniles with high doses of both hormones irreversibly shifts the corresponding hormone status for a period well beyond the time scale for total degradation of the injected hormone. The hormones program the ossification of the jaw suspension bones and neurocranial elements in a specific manner affecting the jaws position and pharingo-branchial area stretching. These morphological shifts resemble the adaptive variants found in sympatric pelagic and demersal morphs of salmonids. We conclude that solitary deviations in the regulators of calcium metabolism could determine functional morphological traits via transformations in skeletal development.     

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.     

An experimental study of the multiple effects of brown trout Salmo trutta on the bioenergetics of two Arctic charr Salvelinus alpinus morphs

This study investigated the importance of competition with brown trout Salmo trutta as a driver of the morphological and behavioural divergence of two morphs of Arctic charr Salvelinus alpinus. The morphs originated from two lakes differing in absence or presence of the competitor. The bioenergetics and behaviour of S. alpinus were quantified in replicate experimental enclosures (mean volume: 150 m(3) ) stocked with 15 S. alpinus of one morph or the other and in the absence or presence of nine S. trutta. The presence of S. trutta decreased growth rate, affected food consumption and increased activity costs in S. alpinus, but provided little support for the hypothesis that competition with S. trutta is a major driver of the divergence of the two S. alpinus morphs. Both morphs responded similarly in terms of mean growth and consumption rates per enclosure, but the association between individual morphology and growth rate reversed between allopatric and sympatric enclosures. While the activity patterns of the two morphs were unaffected by the presence of S. trutta, their swimming speed and activity rate differed. Since the profound differences in the structure of the physical habitat of the source lakes provided a more likely explanation for the difference observed among these two morphs than interspecific competition, it is hypothesized that physical habitat may sometimes be a significant driving force of the phenotypic divergence.     

Phenotypic divergence among threespine stickleback that differ in nuptial coloration

By studying systems in their earliest stages of differentiation, we can learn about the evolutionary forces acting within and among populations and how those forces could contribute to reproductive isolation. Such an understanding would help us to better discern and predict how selection leads to the maintenance of multiple morphs within a species, rather than speciation. The postglacial adaptive radiation of the threespine stickleback (Gasterosteus aculeatus) is one of the best‐studied cases of evolutionary diversification and rapid, repeated speciation. Following deglaciation, marine stickleback have continually invaded freshwater habitats across the northern hemisphere and established resident populations that diverged innumerable times from their oceanic ancestors. Independent freshwater colonization events have yielded broadly parallel patterns of morphological differences in freshwater and marine stickleback. However, there is also much phenotypic diversity within and among freshwater populations. We studied a lesser‐known freshwater “species pair” found in southwest Washington, where male stickleback in numerous locations have lost the ancestral red sexual signal and instead develop black nuptial coloration. We measured phenotypic variation in a suite of traits across sites where red and black stickleback do not overlap in distribution and at one site where they historically co‐occurred. We found substantial phenotypic divergence between red and black morphs in noncolor traits including shape and lateral plating, and additionally find evidence that supports the hypothesis of sensory drive as the mechanism responsible for the evolutionary switch in color from red to black. A newly described third “mixed” morph in Connor Creek, Washington, differs in head shape and size from the red and black morphs, and we suggest that their characteristics are most consistent with hybridization between anadromous and freshwater stickleback. These results lay the foundation for future investigation of the underlying genetic basis of this phenotypic divergence as well as the evolutionary processes that may drive, maintain, or limit divergence among morphs.     

Characterizing neutral and adaptive genomic differentiation in a changing climate: The most northerly freshwater fish as a model

Arctic freshwater ecosystems have been profoundly affected by climate change. Given that the Arctic charr (Salvelinus alpinus) is often the only fish species inhabiting these ecosystems, it represents a valuable model for studying the impacts of climate change on species life‐history diversity and adaptability. Using a genotyping‐by‐sequencing approach, we identified 5,976 neutral single nucleotide polymorphisms and found evidence for reduced gene flow between allopatric morphs from two high Arctic lakes, Linne'vatn (Anadromous, Normal, and Dwarf) and Ellasjøen (Littoral and Pelagic). Within each lake, the degree of genetic differentiation ranged from low (Pelagic vs. Littoral) to moderate (Anadromous and Normal vs. Dwarf). We identified 17 highly diagnostic, putatively adaptive SNPs that differentiated the allopatric morphs. Although we found no evidence for adaptive differences between morphs within Ellasjøen, we found evidence for moderate (Anadromous vs. Normal) to high genetic differentiation (Anadromous and Normal vs. Dwarf) among morphs within Linne'vatn based on two adaptive loci. As these freshwater ecosystems become more productive, the frequency of sympatric morphs in Ellasjøen will likely shift based on foraging opportunities, whereas the propensity to migrate may decrease in Linne'vatn, increasing the frequency of the Normal morph. The Dwarf charr was the most genetically distinct group. Identifying the biological basis for small body size should elucidate the potential for increased growth and subsequent interbreeding with sympatric morphs. Overall, neutral and adaptive genomic differentiation between allopatric and some sympatric morphs suggests that the response of Arctic charr to climate change will be variable across freshwater ecosystems.     

Ecological differences between hamlet (Hypoplectrus: Serranidae) colour morphs: between-morph variation in diet

Dietary differences between hamlet Hypoplectrus spp. colour morphs were examined in fishes from Puerto Rico, U.S. Virgin Islands, Curacao, Honduras and Belize. Hamlet diet across all countries was characterized by large overlap between most colour morphs in both the proportion and numbers of dietary items consumed, although some differences between morphs were apparent. Indigo hamlets Hypoplectrus indigo were the only morph to consume fishes (blue chromis Chromis cyanea and sunshinefish Chromis insolata ) almost exclusively. The sympatric occurrence of other ecologically indistinguishable colour morphs, however, suggests that divergent ecological selection alone cannot explain population divergence in hamlets. Geographical variation in diet was also observed within black Hypoplectrus nigricans and yellowtail Hypoplectrus chlorurus hamlets which may reflect geographical differences in prey availability or differences in prey choice.     

Patterns of morphological changes and hybridization between sympatric whitefish morphs (Coregonus spp.) in a Swiss lake: a role for eutrophication?

Whitefish, genus Coregonus, show exceptional levels of phenotypic diversity with sympatric morphs occurring in numerous postglacial lakes in the northern hemisphere. Here, we studied the effects of human‐induced eutrophication on sympatric whitefish morphs in the Swiss lake, Lake Thun. In particular, we addressed the questions whether eutrophication (i) induced hybridization between two ecologically divergent summer‐spawning morphs through a loss of environmental heterogeneity, and (ii) induced rapid adaptive morphological changes through changes in the food web structure. Genetic analysis based on 11 microsatellite loci of 282 spawners revealed that the pelagic and the benthic morph represent highly distinct gene pools occurring at different relative proportions on all seven known spawning sites. Gill raker counts, a highly heritable trait, showed nearly discrete distributions for the two morphs. Multilocus genotypes characteristic of the pelagic morph had more gill rakers than genotypes characteristic of benthic morph. Using Bayesian methods, we found indications of recent but limited introgressive hybridization. Comparisons with historical gill raker data yielded median evolutionary rates of 0.24 haldanes and median selection intensities of 0.27 for this trait in both morphs for 1948–2004 suggesting rapid evolution through directional selection at this trait. However, phenotypic plasticity as an alternative explanation for this phenotypic change cannot be discarded. We hypothesize that both the temporal shifts in mean gill raker counts and the recent hybridization reflect responses to changes in the trophic state of the lake induced by pollution in the 1960s, which created novel selection pressures with respect to feeding niches and spawning site preferences.     

Lack of parallel genetic patterns underlying the repeated ecological divergence of beach and stream‐spawning kokanee salmon

Recent progress in methods for detecting adaptive population divergence in situ shows promise for elucidating the conditions under which selection acts to generate intraspecific diversity. Rapid ecological diversification is common in fishes; however, the role of phenotypic plasticity and adaptation to local environments is poorly understood. It is now possible to investigate genetic patterns to make inferences regarding phenotypic traits under selection and possible mechanisms underlying ecotype divergence, particularly where similar novel phenotypes have arisen in multiple independent populations. Here, we employed a bottom‐up approach to test for signatures of directional selection associated with divergence of beach‐ and stream‐spawning kokanee, the obligate freshwater form of sockeye salmon (Oncorhynchus nerka). Beach‐ and stream‐spawners co‐exist in many post‐glacial lakes and exhibit distinct reproductive behaviours, life‐history traits and spawning habitat preferences. Replicate ecotype pairs across five lakes in British Columbia, Canada were genotyped at 57 expressed sequence tag‐linked and anonymous microsatellite loci identified in a previous genome scan. Fifteen loci exhibited signatures of directional selection (high F_ST outliers), four of which were identified in multiple lakes. However, the lack of parallel genetic patterns across all lakes may be a result of: 1) an inability to detect loci truly under selection; 2) alternative genetic pathways underlying ecotype divergence in this system; and/or 3) phenotypic plasticity playing a formative role in driving kokanee spawning habitat differences. Gene annotations for detected outliers suggest pathogen resistance and energy metabolism as potential mechanisms contributing to the divergence of beach‐ and stream‐spawning kokanee, but further study is required.     

A single mitochondrial haplotype and nuclear genetic differentiation in sympatric colour morphs of a riverine cichlid fish

Some of the diversity of lacustrine cichlid fishes has been ascribed to sympatric divergence, whereas diversification in rivers is generally driven by vicariance and geographic isolation. In the riverine Pseudocrenilabrus philander species complex, several morphologically highly distinct populations are restricted to particular river systems, sinkholes and springs in southern Africa. One of these populations consists of a prevalent yellow morph in sympatry with a less frequent blue morph, and no individuals bear intermediate phenotypes. Genetic variation in microsatellites and AFLP markers was very low in both morphs and one single mtDNA haplotype was fixed in all samples, indicating a very young evolutionary age and small effective population size. Nevertheless, the nuclear markers detected low but significant differentiation between the two morphs. The data suggest recent and perhaps sympatric divergence in the riverine habitat.     

Ecological and evolutionary consequences of the trophic polymorphism in Cichlasoma citrinellum (Pisces: Cichlidae)

The neotropical cichlid fish Cichlasoma citrinellum is polymorphic in the structure of its pharyngeal jaw apparatus and external morphology. The pharyngeal jaws are either gracile and bear slender, pointed teeth (papilliform) or robust with strong, rounded teeth (molariform). Molariform morphs have a ‘benthic’, and papilliform morphs a ‘limnetic’ body form. Furthermore, this species is also polychromatic, with yellow and black morphs. The molariform morphology of the pharyngeal jaw apparatus adapts the fish for cracking and feeding on snails. Based on analysis of stomach contents, 94% of the molariform morph ate snails whereas only 19%, of the papilliform morph did so. This result suggests that the morphs occupy different ecological niches. The morphology of the pharyngeal jaw apparatus does not correlate significantly with sex, but it does with body colouration (P<0.005). Cichlasoma citrinellum mate assortatively with their own colour; therefore a mating preference for colour may lead to genetic isolation of trophic morphs. The frequency of the molariform morph differs strikingly among populations of five Nicaraguan lakes and its abundance is correlated with the abundance of snails, the fishes' principal prey item. Among populations the frequency of molariform morphs decreases in the dry season. Morphology possibly changes reversibly within particular individuals between seasons. These results suggest that phenotypic plasticity and polymorphisms may be an adaptive characteristic of cichlid fishes. Patterns of intraspecific morphological variation match patterns of interspecific morphological diversification which suggests that universal developmental mechanisms canalize the possible expressions of morphology. The ability to respond morphologically to environmental shifts, in conjunction with genetically determined trophic polymorphisms and sexual selection via mate choice, could be the basis for speciation through intermediate stages of polymorphism of the impressive adaptive radiation of cichlid fishes.