Selection on the morphology–physiology‐performance nexus: Lessons from freshwater stickleback morphs

Conspecifics inhabiting divergent environments frequently differ in morphology, physiology, and performance, but the interrelationships amongst traits and with Darwinian fitness remains poorly understood. We investigated population differentiation in morphology, metabolic rate, and swimming performance in three‐spined sticklebacks (Gasterosteus aculeatus L.), contrasting a marine/ancestral population with two distinct freshwater morphotypes derived from it: the “typical” low‐plated morph, and a unique “small‐plated” morph. We test the hypothesis that similar to plate loss in other freshwater populations, reduction in lateral plate size also evolved in response to selection. Additionally, we test how morphology, physiology, and performance have evolved in concert as a response to differences in selection between marine and freshwater environments. We raised pure‐bred second‐generation fish originating from three populations and quantified their lateral plate coverage, burst‐ and critical swimming speeds, as well as standard and active metabolic rates. Using a multivariate Q_ST‐F_ST framework, we detected signals of directional selection on metabolic physiology and lateral plate coverage, notably demonstrating that selection is responsible for the reduction in lateral plate coverage in a small‐plated stickleback population. We also uncovered signals of multivariate selection amongst all bivariate trait combinations except the two metrics of swimming performance. Divergence between the freshwater and marine populations exceeded neutral expectation in morphology and in most physiological and performance traits, indicating that adaptation to freshwater habitats has occurred, but through different combinations of traits in different populations. These results highlight both the complex interplay between morphology, physiology and performance in local adaptation, and a framework for their investigation.     

Lateral plate number in low‐plated threespine stickleback: a study of plasticity and heritability

In the threespine stickleback Gasterosteus aculeatus model system, phenotypes are often classified into three morphs according to lateral plate number. Morph identity has been shown to be largely genetically determined, but substantial within‐morph variation in plate number exists. In this study, we test whether plate number has a plastic component in response to salinity in the low‐plated morph using a split‐clutch experiment where families were split in two, one half raised in water at 0 and the other at 30 ppt salt. We find a small salinity‐induced plastic effect on plate number in an unexpected direction, opposite to what we predicted: Fish raised in freshwater on average have slightly more plates than fish raised in saltwater. Our results confirm that heritability of plate number is high. Additionally, we find that variance in plate number at the family level can be predicted from other family level traits, which might indicate that epistatic interactions play a role in creating the observed pattern of lateral plate number variation.     

A gene with major phenotypic effects as a target for selection vs. homogenizing gene flow

Genes with major phenotypic effects facilitate quantifying the contribution of genetic vs. plastic effects to adaptive divergence. A classical example is Ectodysplasin (Eda), the major gene controlling lateral plate phenotype in three‐spined stickleback. Completely plated marine stickleback populations evolved repeatedly towards low‐plated freshwater populations, representing a prime example of parallel evolution by natural selection. However, many populations remain polymorphic for lateral plate number. Possible explanations for this polymorphism include relaxation of selection, disruptive selection or a balance between divergent selection and gene flow. We investigated 15 polymorphic stickleback populations from brackish and freshwater habitats in coastal North‐western Europe. At each site, we tracked changes in allele frequency at the Eda gene between subadults in fall, adults in spring and juveniles in summer. Eda genotypes were also compared for body size and reproductive investment. We observed a fitness advantage for the Eda allele for the low morph in freshwater and for the allele for the complete morph in brackish water. Despite these results, the differentiation at the Eda gene was poorly correlated with habitat characteristics. Neutral population structure was the best predictor of spatial variation in lateral plate number, suggestive of a substantial effect of gene flow. A meta‐analysis revealed that the signature of selection at Eda was weak compared to similar studies in stickleback. We conclude that a balance between divergent selection and gene flow can maintain stickleback populations polymorphic for lateral plate number and that ecologically relevant genes may not always contribute much to local adaptation, even when targeted by selection.     

MULTIPLE EVOLUTIONARY PATHWAYS TO DECREASED LATERAL PLATE COVERAGE IN FRESHWATER THREESPINE STICKLEBACKS

Adaptation to novel environments can be based either on standing genetic variation or variation attributable to new mutations. When standing genetic variation for a functional adaptation is lacking, and variation due to new mutations is not yet available, adaptation is possible only through alternative functional solutions. Reduction in the number of bony lateral plates as an adaptation to freshwater colonization by marine threespine sticklebacks (Gasterosteus aculeatus) has occurred in numerous independent cases through allelic substitution in the ectodysplasin‐a (Eda) gene. Studying the phenotypic and genetic variation in plate number and size in five marine and six freshwater threespine stickleback populations, we found that when variation in Eda was limiting (i.e., alleles associated with the low‐plate morph were missing or in extremely low frequency), plate number reduction did not take place in freshwater populations, but reduced lateral plate coverage was achieved by a reduction in the size of lateral plates. Our results suggest that this phenotypically and genetically discrete "small‐plated" threespine stickleback—which is the dominant form in three northern European freshwater populations—may be functionally equivalent to the low‐plated morph and hence, serve as an example of convergent evolution toward functional similarity in the face of genetic constraints.     

Phylogeography and adaptation genetics of stickleback from the Haida Gwaii archipelago revealed using genome‐wide single nucleotide polymorphism genotyping

Threespine stickleback populations are model systems for studying adaptive evolution and the underlying genetics. In lakes on the Haida Gwaii archipelago (off western Canada), stickleback have undergone a remarkable local radiation and show phenotypic diversity matching that seen throughout the species distribution. To provide a historical context for this radiation, we surveyed genetic variation at >1000 single nucleotide polymorphism (SNP) loci in stickleback from over 100 populations. SNPs included markers evenly distributed throughout genome and candidate SNPs tagging adaptive genomic regions. Based on evenly distributed SNPs, the phylogeographic pattern differs substantially from the disjunct pattern previously observed between two highly divergent mtDNA lineages. The SNP tree instead shows extensive within watershed population clustering and different watersheds separated by short branches deep in the tree. These data are consistent with separate colonizations of most watersheds, despite underlying genetic connections between some independent drainages. This supports previous suppositions that morphological diversity observed between watersheds has been shaped independently, with populations exhibiting complete loss of lateral plates and giant size each occurring in several distinct clades. Throughout the archipelago, we see repeated selection of SNPs tagging candidate freshwater adaptive variants at several genomic regions differentiated between marine–freshwater populations on a global scale (e.g. EDA, Na/K ATPase). In estuarine sites, both marine and freshwater allelic variants were commonly detected. We also found typically marine alleles present in a few freshwater lakes, especially those with completely plated morphology. These results provide a general model for postglacial colonization of freshwater habitat by sticklebacks and illustrate the tremendous potential of genome‐wide SNP data sets hold for resolving patterns and processes underlying recent adaptive divergences.     

Allometric relationships in morphological traits associated with foraging,swimming ability,and predator defense reveal adaptations toward brackish and freshwater environments in the threespine stickleback

Freshwater colonization by threespine stickleback has led to divergence in morphology between ancestral marine and derived freshwater populations, making them ideal for studying natural selection on phenotypes. In an open brackish–freshwater system, we previously discovered two genetically distinct stickleback populations that also differ in geometric shape: one mainly found in the brackish water lagoon and one throughout the freshwater system. As shape and size are not perfectly correlated, the aim of this study was to identify the morphological trait(s) that separated the populations in geometric shape. We measured 23 phenotypes likely to be important for foraging, swimming capacity, and defense against predation. The lateral plate morphs in freshwater displayed few significant changes in trait sizes, but the low plated expressed feeding traits more associated with benthic habitats. When comparing the completely plated genetically assigned populations, the freshwater, the hybrids, the migrants and the lagoon fish, many of the linear traits had different slopes and intercepts in trait‐size regressions, precluding our ability to directly compare all traits simultaneously, which most likely results from low variation in body length for the lagoon and migrant population. We found the lagoon stickleback population to be more specialized toward the littoral zone, displaying benthic traits such as large, deep bodies with smaller eyes compared to the freshwater completely plated morph. Further, the lagoon and migrant fish had an overall higher body coverage of lateral plates compared to freshwater fish, and the dorsal and pelvic spines were longer. Evolutionary constraints due to allometric scaling relationships could explain the observed, overall restricted, differences in morphology between the sticklebacks in this study, as most traits have diversified in common allometric trajectories. The observed differences in foraging and antipredation traits between the fish with a lagoon and freshwater genetic signature are likely a result of genetic or plastic adaptations toward brackish and freshwater environments.     

Body armour and lateral‐plate reduction in freshwater three‐spined stickleback Gasterosteus aculeatus: adaptations to a different buoyancy regime?

Several factors related to buoyancy were compared between one marine and two freshwater populations of three‐spined stickleback Gasterosteus aculeatus. Fish from all three populations had buoyancy near to neutral to the ambient water. This showed that neither marine nor freshwater G. aculeatus used swimming and hydrodynamic lift to prevent sinking. Comparing the swimbladder volumes showed that freshwater completely plated G. aculeatus had a significantly larger swimbladder volume than both completely plated marine and low‐plated freshwater G. aculeatus. Furthermore, body tissue density was lower in low‐plated G. aculeatus than in the completely plated marine and freshwater fish. The results show that G. aculeatus either reduce tissue density or increase swimbladder volume to adapt to lower water density. Mass measurements of lateral plates and pelvis showed that loss of body armour in low‐plated G. aculeatus could explain the tissue density difference between low‐plated and completely plated G. aculeatus. This suggests that the common occurrence of plate and armour reduction in freshwater G. aculeatus populations can be an adaptation to a lower water density.     

Water temperature,not fish morph,determines parasite infections of sympatric Icelandic threespine sticklebacks (Gasterosteus aculeatus)

Parasite communities of fishes are known to respond directly to the abiotic environment of the host, for example, to water quality and water temperature. Biotic factors are also important as they affect the exposure profile through heterogeneities in parasite distribution in the environment. Parasites in a particular environment may pose a strong selection on fish. For example, ecological differences in selection by parasites have been hypothesized to facilitate evolutionary differentiation of freshwater fish morphs specializing on different food types. However, as parasites may also respond directly to abiotic environment the parasite risk does not depend only on biotic features of the host environment. It is possible that different morphs experience specific selection gradients by parasites but it is not clear how consistent the selection is when abiotic factors change. We examined parasite pressure in sympatric morphs of threespine stickleback (Gasterosteus aculeatus) across a temperature gradient in two large Icelandic lakes, Myvatn and Thingvallavatn. Habitat‐specific temperature gradients in these lakes are opposite. Myvatn lava rock morph lives in a warm environment, while the mud morph lives in the cold. In Thingvallavatn, the lava rock morph lives in a cold environment and the mud morph in a warm habitat. We found more parasites in fish living in higher temperature in both lakes, independent of the fish morph, and this pattern was similar for the two dominating parasite taxa, trematodes and cestodes. However, at the same time, we also found higher parasite abundance in a third morph living in deep cold–water habitat in Thingvallavatn compared to the cold‐water lava morph, indicating strong effect of habitat‐specific biotic factors. Our results suggest complex interactions between water temperature and biotic factors in determining the parasite community structure, a pattern that may have implications for differentiation of stickleback morphs.     

High levels of interspecific gene flow in an endemic cichlid fish adaptive radiation from an extreme lake environment

Studying recent adaptive radiations in isolated insular systems avoids complicating causal events and thus may offer clearer insight into mechanisms generating biological diversity. Here, we investigate evolutionary relationships and genomic differentiation within the recent radiation of Alcolapia cichlid fish that exhibit extensive phenotypic diversification, and which are confined to the extreme soda lakes Magadi and Natron in East Africa. We generated an extensive RAD data set of 96 individuals from multiple sampling sites and found evidence for genetic admixture between species within Lake Natron, with the highest levels of admixture between sympatric populations of the most recently diverged species. Despite considerable environmental separation, populations within Lake Natron do not exhibit isolation by distance, indicating panmixia within the lake, although individuals within lineages clustered by population in phylogenomic analysis. Our results indicate exceptionally low genetic differentiation across the radiation despite considerable phenotypic trophic variation, supporting previous findings from smaller data sets; however, with the increased power of densely sampled SNPs, we identify genomic peaks of differentiation (F_ST outliers) between Alcolapia species. While evidence of ongoing gene flow and interspecies hybridization in certain populations suggests that Alcolapia species are incompletely reproductively isolated, the identification of outlier SNPs under diversifying selection indicates the radiation is undergoing adaptive divergence.     

Twelve years of contemporary armor evolution in a threespine stickleback population

Abstract —Loberg Lake, Alaska was colonized by sea-run Gasterosteus aculeatus between 1983 and 1988, after the original stickleback population was exterminated. Annual samples from 1990 to 2001 reveal substantial evolution of lateral plate (armor) phenotypes. The 1990 sample was nearly monomorphic for the complete plate morph, which is monomorphic in local sea-run populations; the low plate morph, which is usually monomorphic in local freshwater populations, was absent. By 2001, the frequency of completes had declined to 11%, and lows had increased to 75%. The partial plate morph and two unusual intermediate plate phenotypes were generally rare, but occurrence of the intermediates was unexpected. These intermediate phenotypes rarely occur in other, presumably older, polymorphic populations. When low morphs first appeared, they averaged 6.8 plates per side, indicating that the ancestral plate number of low morphs is high, and their mean has subsequently declined. Contemporary evolution in this population indicates that threespine stickleback adapt to freshwater habitats within decades after invasion from the ocean, and thus phenotypes in most populations are adapted to current conditions.     

Allopatric and sympatric diversification within roach (Rutilus rutilus) of large pre‐alpine lakes

Intraspecific differentiation in response to divergent natural selection between environments is a common phenomenon in some northern freshwater fishes, especially salmonids and stickleback. Understanding why these taxa diversify and undergo adaptive radiations while most other fish species in the same environments do not, remains an open question. The possibility for intraspecific diversification has rarely been evaluated for most northern freshwater fish species. Here, we assess the potential for intraspecific differentiation between and within lake populations of roach (Rutilus rutilus)—a widespread and abundant cyprinid species—in lakes in which salmonids have evolved endemic adaptive radiations. Based on more than 3,000 polymorphic RADseq markers, we detected low but significant genetic differentiation between roach populations of two ultraoligotrophic lakes and between these and populations from other lakes. This, together with differentiation in head morphology and stable isotope signatures, suggests evolutionary and ecological differentiation among some of our studied populations. Next, we tested for intralacustrine diversification of roach within Lake Brienz, the most pristine lake surveyed in this study. We found significant phenotypic evidence for ecological intralacustrine differentiation between roach caught over a muddy substrate and those caught over a rocky substrate. However, evidence for intralacustrine genetic differentiation is at best subtle and phenotypic changes may therefore be mostly plastic. Overall, our findings suggest roach can differ between ecologically distinct lakes, but the extent of intralacustrine ecological differentiation is weak, which contrasts with the strong differentiation among endemic species of whitefish in the same lakes.     

近期引入三刺鱼种群的骨板和体型的现时进化

近期引入到新环境中的种群给我们提供了一个推论种群过去微进化变化的难得的机会,而这些变化曾导致了种群在历史上对新栖息地拓殖的适应。自从1967年三刺鱼(GasterosteusaculeatusL.)被有意引入到不列颠哥伦比亚的Heisholt湖后,就隔离的淡水对其完全骨板化(CP)变体的相对适合度的影响已经做过多种多样的测定。CP变体的个体在早期的样本中比较常见(占20.3%-31.7%),而在现代的样本中比较稀少(占0%-5.0%)。后者样本中骨板弱化的变体占优势,这是绝大多数淡水种群的典型情形。我估测Heisholt湖的一个流域中三刺鱼体侧骨板数目从1974年到1997年的进化速率是-0.029海尔登,这比大多数对近期引入的或隔离的三刺鱼种群的现时进化的估测要低。最后,来自于Heisholt湖的CP个体比那些作为引入源溪流中的个体明显要小。总之,对应于已建群的自然淡水种群的文献资料,在引入种群中所观察到的个体大小和体侧骨板数目的变化,意味着三刺鱼对与淡水环境中生活相关的多种挑战的适应可以快速发生。     

Geographical variations in freshwater populations of the three-spined stickleback,Gasterosteus aculeatus,in Japan

This paper describes an investigation of morphological variation among six freshwater populations (dominantly low-plated morph) of the three-spined stickleback,Gasterosteus aculeatus, in Japan. Such populations are mainly distributed in restricted water areas within a band from Ise to Wakasa Bays, the most constricted part of Honshu Island. According to some differences in morphological variation, i.e. plate morph, number of lateral plates, body size, body shape and body colour, they were classified into two types corresponding to occurrence in the Ibi River and Lake Biwa water systems. The former type was monomorphic dominated by lowplated morphs in spring-fed water, whereas the latter was a dimorphic population consisting of low- and partially-plated morphs. My results suggest that the plate morph type is not correlated with climate nor predation but is related to geological isolation patterns during the course of the landlocking process. Conversely, variations in meristic (number of dorsal and anal fin rays and gill rakers) and morphometric (body shape and body colour) characteristics may have been related to different environmental conditions. This study also provides supporting evidence that the freshwater three-spined stickleback is a distinct species from the anadromous stickleback,G. aculeatus.     

Watershed characteristics shape the landscape genetics of brook stickleback (Culaea inconstans) in shallow prairie lakes

Investigating the consequences of landscape features on population genetic patterns is increasingly important to elucidate the ecological factors governing connectivity between populations and predicting the evolutionary consequences of landscapes. Small prairie lakes in Alberta, Canada, and the brook stickleback (Culaea inconstans) that inhabit them, provide a unique aquatic system whereby populations are highly isolated from one another. These heterogeneous and extreme environments are prone to winterkills, an event whereby most of the fish die and frequent bottlenecks occur. In this study, we characterized the genetic population structure of brook stickleback among several lakes, finding that the species is hierarchically influenced by within‐lake characteristics in small‐scale watersheds. Landscape genetic analyses of the role of spatial features found support for basin characteristics associated with genetic diversity and bottlenecks in 20% of the sampled lakes. These results suggest that brook stickleback population genetic patterns may be driven, at least in part, by ecological processes that accelerate genetic drift and landscape patterns associated with reduced dispersal. Collectively, these results reinforce the potential importance of connectivity in the maintenance of genetic diversity, especially in fragmented landscapes.     

Non‐parallel divergence across freshwater and marine three‐spined stickleback Gasterosteus aculeatus populations

This work investigated whether multiple freshwater populations of three‐spined stickleback Gasterosteus aculeatus in different freshwater catchments in the Jutland Peninsula, Denmark, derived from the same marine populations show repeated adaptive responses. A total of 327 G. aculeatus collected at 13 sampling locations were screened for genetic variation using a combination of 70 genes putatively under selection and 26 neutral genes along with a marker linked to the ectodysplasin gene (eda), which is strongly correlated with plate armour morphs in the species. A highly significant genetic differentiation was found that was higher among different freshwater samples than between marine–freshwater samples. Tests for selection between marine and freshwater populations showed a very low degree of parallelism and no single nucleotide polymorphism was detected as outlier in all freshwater–marine pairwise comparisons, including the eda. This suggests that G. aculeatus is not necessarily the prime example of parallel local adaptation suggested in much of the literature and that important exceptions exist (i.e. the Jutland Peninsula). While marine populations in the results described here showed a high phenotype–genotype correlation at eda, a low association was found for most of the freshwater populations. The most extreme case was found in the freshwater Lake Hald where all low‐plated phenotypes were either homozygotes for the allele supposed to be associated with completely plated morphs or heterozygotes, but none were homozygotes for the putative low‐plated allele. Re‐examination of data from seven G. aculeatus studies agrees in showing a high but partial association between phenotype–genotype at eda in G. aculeatus freshwater populations and that mismatches occur everywhere in the European regions studied (higher in some areas, i.e. Denmark). This is independent of the eda marker used.     

The utility of QTL-Linked markers to detect selective sweeps in natural populations--a case study of the EDA gene and a linked marker in threespine stickleback

Sequence polymorphisms in coding genes and variability in quantitative trait loci (QTL)-linked markers can be used to uncover the evolutionary mechanisms of traits involved in adaptive processes. We studied sequence variation in the EDA gene and allelic variation in 18 microsatellites - one of which (Gac4174) is linked with the EDA QTL - in low, partially and completely plated morphs from eight threespine stickleback European populations. The results agree with previous studies in that EDA polymorphism is closely related to plate number variation: EDA sequences grouped populations into low and completely plated morphs, whereas microsatellites failed to do so. Furthermore, partially plated fish were heterozygous with respect to the distinctive EDA alleles for completely and low plated morphs, indicating that completely plated morph alleles are not entirely dominant in controlling the expression of lateral plate number. An examination of population differentiation in plate number with quantitative genetic methods revealed that the degree of differentiation exceeded that expected from genetic drift alone (Q(ST) > F(ST)). Our results support the adaptive genetic differentiation of plate morphs and the view that distinctive EDA gene polymorphism occurs in similar sites across the distribution range of this species. Yet, allele frequency differentiation in the Gac4174 microsatellite locus, informative in experimental crosses for plate number variation, did not differ from that of neutral markers and, was therefore unable to detect the signature of natural selection responsible for population 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.     

Climate‐driven habitat change causes evolution in Threespine Stickleback

Climate change can shape evolution directly by altering abiotic conditions or indirectly by modifying habitats, yet few studies have investigated the effects of climate‐driven habitat change on contemporary evolution. We resampled populations of Threespine Stickleback (Gasterosteus aculeatus) along a latitudinal gradient in California bar‐built estuaries to examine their evolution in response to changing climate and habitat. We took advantage of the strong association between stickleback lateral plate phenotypes and Ectodysplasin A (Eda) genotypes to infer changes in allele frequencies over time. Our results show that over time the frequency of low‐plated alleles has generally increased and heterozygosity has decreased. Latitudinal patterns in stickleback plate phenotypes suggest that evolution at Eda is a response to climate‐driven habitat transformation rather than a direct consequence of climate. As climate change has reduced precipitation and increased temperature and drought, bar‐built estuaries have transitioned from lotic (flowing‐water) to lentic (still‐water) habitats, where the low‐plated allele is favoured. The low‐plated allele has achieved fixation at the driest, hottest southernmost sites, a trend that is progressing northward with climate change. Climate‐driven habitat change is therefore causing a reduction in genetic variation that may hinder future adaptation for populations facing multiple threats.     

The role of calcium and predation on plate morph evolution in the three‐spined stickleback (Gasterosteus aculeatus)

While the genetic basis to plate morph evolution of the three‐spined stickleback (Gasterosteus aculeatus) is well described, the environmental variables that select for different plate and spine morphs are incompletely understood. Using replicate populations of three‐spined sticklebacks on North Uist, Scotland, we previously investigated the role of predation pressure and calcium limitation on the adaptive evolution of stickleback morphology and behavior. While dissolved calcium proved a significant predictor of plate and spine morph, predator abundance did not. Ecol. Evol., xxx, 2014 and xxx performed a comparable analysis to our own to address the same question. They failed to detect a significant effect of dissolved calcium on morphological evolution, but did establish a significant effect of predation; albeit in the opposite direction to their prediction.     

Resource diversity promotes among‐individual diet variation,but not genomic diversity,in lake stickleback

Many generalist species consist of specialised individuals that use different resources. This within‐population niche variation can stabilise population and community dynamics. Consequently, ecologists wish to identify environmental settings that promote such variation. Theory predicts that environments with greater resource diversity favour ecological diversity among consumers (via disruptive selection or plasticity). Alternatively, niche variation might be a side‐effect of neutral genomic diversity in larger populations. We tested these alternatives in a metapopulation of threespine stickleback. Stickleback consume benthic and limnetic invertebrates, focusing on the former in small lakes, the latter in large lakes. Intermediate‐sized lakes support generalist stickleback populations using an even mixture of the two prey types, and exhibit greater among‐individual variation in diet and morphology. In contrast, genomic diversity increases with lake size. Thus, phenotypic diversity and neutral genetic polymorphism are decoupled: trophic diversity being greatest in intermediate‐sized lakes with high resource diversity, whereas neutral genetic diversity is greatest in the largest lakes.