Evolutionary diversification of opercle shape in Cook Inlet threespine stickleback

We investigated the evolution of a large facial bone, the opercle (OP), in lake populations of the threespine stickleback that were founded by anadromous ancestors, in Cook Inlet, Alaska. Recent studies characterized OP variation among marine and lake populations and mapped a quantitative trait locus with a large influence on OP shape. Using populations from diverse environments and independent evolutionary histories, we examined divergence of OP shape from that of the anadromous ancestor. We report preliminary evidence for divergence between benthic and generalist lake ecotypes, necessitating further investigation. Furthermore, rapid divergence of OP shape has occurred in a lake population that was founded by anadromous stickleback in the 1980s, which is consistent with divergence of other phenotypic traits and with OP diversification in other lake populations. By contrast, there has been limited evolution of OP shape in a second lake population that may have experienced a genetic bottleneck early in its history and lacks genetic variation for OP divergence. Taken together, the results obtained from these two populations are consistent with studies of other stickleback phenotypic traits that implicate ancestral variation in postglacial adaptive radiation of threespine stickleback in fresh water.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 832–844.     

Morphological divergence patterns among populations of Poecilia vivipara (Teleostei Poeciliidae): test of an ecomorphological paradigm

The structure of body size and shape divergence among populations of Poecilia vivipara inhabiting quaternary lagoons in South-eastern Brazil was studied. This species is abundant throughout an environmental gradient formed by water salinity differences. The salinity gradient influences the habitat structure (presence of macrophytes) and the fish community (presence of large predators). Size and shape variation within and among populations was quantified by geometric morphometrics and analysed by indirect and direct gradient ordinations, using salinity and geography as a framework. Morphological divergence was associated with the salinity gradient. The evolutionary allometries observed were independent of within-group static allometries. Sexually dimorphic patterns were observed in size variation and within-population allometries. Specimens from freshwater (higher predation) sites presented smaller sizes, relatively longer caudal regions, lower anterior regions and a ventrally displaced eye. These features are consistent with an ecomorphological paradigm for aquatic organisms from populations subject to intense predation. A process of directional selection is postulated as the most likely force driving diversification among P. vivipara populations.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 93 , 799–812.     

Spatial phenotypic and genetic structure of threespine stickleback (Gasterosteus aculeatus) in a heterogeneous natural system,Lake Mývatn,Iceland

Eco‐evolutionary responses of natural populations to spatial environmental variation strongly depend on the relative strength of environmental differences/natural selection and dispersal/gene flow. In absence of geographic barriers, as often is the case in lake ecosystems, gene flow is expected to constrain adaptive divergence between environments – favoring phenotypic plasticity or high trait variability. However, if divergent natural selection is sufficiently strong, adaptive divergence can occur in face of gene flow. The extent of divergence is most often studied between two contrasting environments, whereas potential for multimodal divergence is little explored. We investigated phenotypic (body size, defensive structures, and feeding morphology) and genetic (microsatellites) structure in threespine stickleback (Gasterosteus aculeatus) across five habitat types and two basins (North and South) within the geologically young and highly heterogeneous Lake Mývatn, North East Iceland. We found that (1) North basin stickleback were, on average, larger and had relatively longer spines than South basin stickleback, whereas (2) feeding morphology (gill raker number and gill raker gap width) differed among three of five habitat types, and (3) there was only subtle genetic differentiation across the lake. Overall, our results indicate predator and prey mediated phenotypic divergence across multiple habitats in the lake, in face of gene flow.     

Ecological opportunity and levels of morphological variance within freshwater stickleback populations

The 'ecological opportunity' hypothesis predicts that when interspecific competition or predation is reduced, populations will exhibit increases in phenotypic variance as a result of colonization and adaptation to vacant or underutilized ecological niches (i.e. character release). We assessed this hypothesis by examining morphological diversity within stickleback populations in 40 undisturbed lakes from six islands off the mid-coast of British Columbia, Canada. Because larger lakes with well-developed littoral and limnetic zones will have greater trophic niche diversity than smaller lakes with only littoral zones, we predicted a positive association between lake size and variation in trophic morphology. Conversely, reduced vertebrate predation in small bog lakes allows increased variance in defensive structures without costs to fitness. Consistent with both predictions, we observed that phenotypic variance in two traits that are involved in feeding (gape width and pectoral fin length) increased with lake size while variability in defence structures (lateral plate number and dorsal spine length) was inversely related to lake size. Moreover, increased variance in defence morphology was accentuated in populations with severe armour reduction (spine loss, decreased plate overlap), another strong indicator of reduced vertebrate predation. In the majority of cases, these patterns were repeatable among islands, independent from the geographical distance between lakes, and arose from a combination of high variance within each of the sexes and increases in sexual dimorphism. These findings suggest that character release can be trait-specific and reflect the combined effects of competition, predation and habitat heterogeneity.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 86 , 297–308.     

Parasite-mediated sexual selection and species divergence in Lake Victoria cichlid fish

We investigate the role of parasite-mediated sexual selection in the divergence of two species of Lake Victoria cichlids. Pundamilia pundamilia and Pundamilia nyererei represent a common pattern of male nuptial colour divergence between haplochromine sister species: metallic grey–blue in P. pundamilia and bright yellow and red in P. nyererei . Female mating preferences for different male colours maintain the genetic and phenotypic differentiation of the two species in clear water. Previous work indicated that the red coloration of P. nyererei males, which is subject to directional sexual selection, may be a carotenoid-dependent signal of parasite infestation rate. In the present study, we find a parallel result for P. pundamilia : bright blue males are infected with fewer species of parasites. We also find that parasite infestation rates differ quantitatively between the two species in a way that is consistent with species differences in diet and microhabitat. We conclude that parasite-mediated sexual selection may have contributed to the divergence of female mating preferences between P. pundamilia and P. nyererei , and may currently strengthen reproductive isolation between these species.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 94 , 53–60.     

A benthic predatory fish does not cause selection on armour traits in three‐spined stickleback Gasterosteus aculeatus (Gasterosteiformes: Gasterosteidae)

Predation can promote divergence between prey populations and contribute to ecological speciation. In theory, predators can also constrain prey population divergence. In coastal British Columbia, Canada, Gasterosteus aculeatus (three‐spined stickleback) species pairs only occur in lakes with a single species of predatory fish: Oncorhynchus clarkii (the cutthroat trout). Similar lakes containing additional predatory fish species (Cottus asper, prickly sculpins; Oncorhynchus mykiss, rainbow trout) contain only single species of morphologically intermediate stickleback, suggesting that these predators prevent the coexistence of stickleback species pairs. We conducted a mesocosm experiment to investigate how prickly sculpins might constrain divergence, by quantifying their impact on survival and natural selection on antipredator (armour) traits in F₂ stickleback from a cross between ecologically divergent populations. We tested three hypotheses: (1) sculpin predation on sticklebacks reduces survival in a way that could result in their exclusion from certain niches; (2) sculpins compete with stickleback; (3) sculpins respond to prey vulnerabilities in similar ways to cutthroat trout, tending to constrain rather than to enhance divergence. We found that sculpins significantly reduce stickleback survival, that their presence per se does not reduce growth in stickleback, and that predation did not result in selection on any of the armour traits measured, or on gill raker length, which is an important trophic trait. These results tend to refute hypotheses (2) and (3), while supporting hypothesis (1). © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 877–885.     

Geographical variation in asymmetry in Gasterosteus aculeatus

We tested whether fluctuating asymmetry (FA) in undisturbed populations is associated with several natural environmental factors and whether FA is negatively correlated with fitness in the wild. We compared the FA of multiple bony structural defences among 87 endemic populations of threespine stickleback ( Gasterosteus aculeatus L.) inhabiting pristine freshwater habitats on the islands of Haida Gwaii, British Columbia, Canada. Multi-trait FA for adults and juvenile fish varied extensively among populations, but only in adults did it correlate with geography and two habitat characteristics (pH and water colour). Mean FA among individual traits varied concordantly among populations but was not correlated within individuals. While asymmetrical fish showed slightly higher levels of parasitism as predicted, selection differentials based on age class comparisons suggested that asymmetrical fish had the same or marginally higher survival than symmetrical fish. Selection differentials of FA varied significantly among traits and may reflect variability in their functional importance and in the strength of selection on their developmental stability. The data imply that FA/fitness associations are heterogeneous and character-specific.  © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 77 , 9–22.     

Microgeographical diversification of threespine stickleback: body shape–habitat correlations in a small, ecologically diverse Alaskan drainage

Adaptive radiations are a major source of evolutionary diversity in nature, and understanding how they originate and how organisms diversify during the early stages of adaptive radiation is a major problem in evolutionary biology. The relationship between habitat type and body shape variation was investigated in a postglacial radiation of threespine stickleback in the upper Fish Creek drainage of Cook Inlet, Alaska. Although small, the upper Fish Creek drainage includes ecologically diverse lakes and streams in close proximity to one another that harbour abundant stickleback. Specimens from ancestral anadromous and derived resident freshwater populations differed substantially and could be distinguished by body shape alone, suggesting that the initial stages of adaptation contribute disproportionately to evolutionary divergence. Body shape divergence among resident freshwater populations was also considerable, and phenotypic distances among samples from freshwater populations were associated with habitat type but not geographical distance. As expected, stream stickleback from slow-moving, structurally complex environments tended to have the deepest bodies, stickleback from lakes with a mostly benthic habitat were similar but less extreme, and stickleback from lakes with a mostly limnetic habitat were the most shallow-bodied, elongate fish. Beyond adapting rapidly to conditions in freshwater environments, stickleback can diversify rapidly over small geographical scales in freshwater systems despite opportunities for gene flow. This study highlights the importance of ecological heterogeneity over small geographical scales for evolutionary diversification during the early stages of adaptive radiation, and lays the foundation for future research on this ecologically diverse, postglacial system.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 139–151.     

Stable isotope niche differentiation in sticklebacks with symmetric and asymmetric pectoral fins

Fluctuating asymmetry (FA) is often, but controversially, viewed as an indicator of fitness and a target of selection. In the brook stickleback, Culaea inconstans (Kirtland), FA of the pectoral fins, which are the main source of propulsion, is inversely correlated with fecundity. We examined the hypothesis that asymmetry of the pectoral fins could affect locomotion in such a way as to influence foraging and niche use in prereproductive brook stickleback. Nitrogen and carbon stable isotope analysis showed the diet of symmetric and asymmetric males diverged with increasing body size. Larger symmetric males fed at higher trophic levels and had a diet based on carbon emanating from a more pelagic source than their asymmetric counterparts. Such effects were not observed in females or smaller males. The number of chironomid larvae found in the gut was greater on average in asymmetric than symmetric fish. The results from this study strongly suggest FA of pectoral fins affects the foraging behaviour of C. inconstans and that stable isotope analyses of individual phenotypes provides a useful tool for assessing the ecological consequences of FA.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 617–623.     

When maladaptive gene flow does not increase selection

Populations receiving high maladaptive gene flow are expected to experience strong directional selection—because gene flow pulls mean phenotypes away from local fitness peaks. We tested this prediction by means of a large and replicated mark‐recapture study of threespine stickleback (Gasterosteus aculeatus) in two stream populations. One of the populations (outlet) experiences high gene flow from the lake population and its morphology is correspondingly poorly adapted. The other population (inlet) experiences very low gene flow from the lake population and its morphology is correspondingly well adapted. Contrary to the above prediction, selection was not stronger in the outlet than in the inlet, a result that forced us to consider potential reasons for why maladaptive gene flow might not increase selection. Of particular interest, we show by means of a simple population genetic model that maladaptive gene flow can—under reasonable conditions—decrease the strength of directional selection. This outcome occurs when immigrants decrease mean fitness in the resident population, which decreases the strength of selection against maladapted phenotypes. We argue that this previously unrecognized effect of gene flow deserves further attention in theoretical and empirical studies.     

Fitness differences between parapatric lake and stream stickleback revealed by a field transplant

Molecular comparisons of populations diverging into ecologically different environments often reveal strong differentiation in localized genomic regions, with the remainder of the genome being weakly differentiated. This pattern of heterogeneous genomic divergence, however, is rarely connected to direct measurements of fitness differences among populations. We here do so by performing a field enclosure experiment in threespine stickleback fish residing in a lake and in three replicate adjoining streams, and displaying weak yet heterogeneous genomic divergence between these habitats. Tracking survival over 29 weeks, we consistently find that lake genotypes transplanted into the streams suffer greatly reduced viability relative to local stream genotypes and that the performance of F1 hybrid genotypes is intermediate. This observed selection against migrants and hybrids combines to a total reduction in gene flow from the lake into streams of around 80%. Overall, our study identifies a strong reproductive barrier between parapatric stickleback populations, and cautions against inferring weak fitness differences between populations exhibiting weak overall genomic differentiation.     

Crosses between frog populations reveal genetic divergence in larval life history at short geographical distance

A number of studies have documented interpopulation divergence in amphibian larval life-history traits across latitudes. Because many frogs are philopatric and have a patchy habitat distribution, genetic divergence could also exist on a much smaller geographical scale, revealed by recent estimates of population divergence using molecular markers. Whether this divergence is reflected in phenotypic traits is virtually unknown. Using artificial fertilization, individuals of the common frog, Rana temporaria , were crossed from two populations situated 130 km apart and differing in population size. The pattern of size at metamorphosis showed evidence of non-additive effects, as demonstrated by a significant interaction between male and female population of origin. Outbreeding resulted in an increase in metamorph size when eggs from the small population were fertilized with sperm from the large population. In the reciprocal cross, however, the pattern was in the opposite direction, with no significant effect of male population of origin. Genetic divergence of populations separated by a relatively short geographical distance may be more common in frogs than previously acknowledged, with potential implications for conservation of declining amphibian species.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 189–195.     

Discordance in body size, colour pattern, and advertisement call across genetically distinct populations in a Neotropical anuran (Dendropsophus ebraccatus)

Patterns of intraspecific geographic variation in morphology and behaviour, when examined in a phylogenetic context, can provide insight into the microevolutionary processes driving population divergence and ultimately speciation. In the present study, we quantified behavioural and phenotypic variation among populations from genetically divergent regions in the Central American treefrog, Dendropsophus ebraccatus . Our fine-scale population comparisons demonstrated regional divergence in body size, colour pattern frequencies, and male advertisement call. None of the characters covaried with phylogenetic history or geographic proximity among sampled populations, indicating the importance of highly localized selection pressures and genetic drift in shaping character divergence among isolated regions. The study underscores how multiple phenotypic characters can evolve independently across relatively small spatial scales.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 298–313.     

Twenty years of body shape evolution in a threespine stickleback population adapting to a lake environment

Analysis of contemporary evolution can provide important insights into the pattern and rate of phenotypic evolution. The threespine stickleback population in Loberg Lake was exterminated in 1982, and a new population was founded between 1983 and 1989 by anadromous stickleback. The body shape of the Loberg Lake population resembled that of anadromous populations in 1990, although it had diverged markedly by 1992. Between 1992 and 2009, the population evolved more slowly to resemble typical lake populations in the region, diverging approximately 68% of the distance separating its putative ancestor and the original native population by 2009. Temporal evolution is the main source of variation, although spatial heterogeneity, armour phenotype, and allometry contribute significant variation. There was no significant effect of ancestral phenotypic shape covariance on the evolutionary trajectory of this population. Temporal variation in the Loberg Lake population provides a rare glimpse into the evolutionary response of a complex trait to natural selection after a major habitat shift. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 817–831.     

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.     

Effects of genetics and light environment on colour expression in threespine sticklebacks

The genetic basis of traits that are under sexual selection and that are involved in recognizing conspecific mates is poorly known, even in systems in which the phenotypic basis of these traits has been well studied. In the present study, we investigate genetic and environmental influences on nuptial colour, which plays important roles in sexual selection and sexual isolation in species pairs of limnetic and benthic threespine sticklebacks ( Gasterosteus aculeatus species complex). Previous work demonstrated that colour differences among species correlate to differences in the ambient light prevalent in their mating habitat. Red fish are found in clear water and black fish in red-shifted habitats. We used a paternal half-sib split-clutch design to investigate the genetic and environmental basis of nuptial colour. We found genetic differences between a red and a black stickleback population in the expression of both red and black nuptial colour. In addition, the light environment influenced colour expression, and genotype by environment interactions were also present. We found evidence for both phenotypic and genetic correlations between our colour traits; some of these correlations are in opposite directions for our red and black populations. These results suggest that both genetic change and phenotypic plasticity underlie the correlation of male colour with light environment.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 663–673.     

Size-dependent mating strategies and the risk of cannibalism

The role of sexual selection in determining the nature and direction of sexual size dimorphism may depend upon the timing of sexual selection, and this may also influence the variation in male size. For example, selection through sperm competition favours smaller males in the highly sexually size dimorphic orb-weaving spider Nephila edulis , whereas larger males are better able to exclude their smaller rivals from the central hub of the web where mating takes place. We investigate experimentally the role of body size and hub tenure in determining male fertilization success when males of different sizes compete for a single female over a 24-h period that includes a period of darkness. Our results confirm that small and large males obtain similar paternity share but that, in contrast with previous studies, hub tenure does not translate into greater paternity share. Unexpectedly, smaller males are at greater risk of postmating sexual cannibalism than larger males, suggesting that natural selection through sexual cannibalism may place a lower limit on male size.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 355–363.     

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.     

Genetic differentiation on multiple spatial scales in an ecotype-forming marine snail with limited dispersal: Littorina saxatilis

The population genetic structure of marine species lacking free-swimming larvae is expected to be strongly affected by random genetic drift among populations, resulting in genetic isolation by geographical distance. At the same time, ecological separation over microhabitats followed by direct selection on those parts of the genome that affect adaptation might also be strong. Here, we address the question of how the relative importance of stochastic vs. selective structuring forces varies at different geographical scales. We use microsatellite DNA and allozyme data from samples of the marine rocky shore snail Littorina saxatilis over distance scales ranging from metres to 1000 km, and we show that genetic drift is the most important structuring evolutionary force at distances > 1 km. On smaller geographical scales (< 1 km), divergent selection between contrasting habitats affects population genetic structure by impeding gene flow over microhabitat borders (microsatellite structure), or by directly favouring specific alleles of selected loci (allozyme structure). The results suggest that evolutionary drivers of population genetic structure cannot a priori be assumed to be equally important at different geographical scales. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 31–40.     

Empirical evaluation of phenotype–environment correlation and trait utility with allopatric and sympatric whitefish, Coregonus lavaretus (L.), populations in subarctic lakes

Adaptive phenotypic divergence of sympatric morphs in a single species may have significant evolutionary consequences. In the present study, phenotypic impacts of predator on zooplankton prey populations were compared in two northern Finnish lakes; one with an allopatric whitefish, Coregonus lavaretus (L.), population and the other with three sympatric whitefish populations. First, we examined whether there were phenotypic associations with specific niches in allopatric and sympatric whitefish. Second, trait utility (i.e. number of gillrakers) of allopatric and sympatric whitefish in utilizing a pelagic resource was explored by comparing predator avoidance of prey, prey size in environment, and prey size in predator diet. The allopatric living large sparsely rakered (LSR) whitefish morph, was a generalist using both pelagic and benthic niches. In contrast, sympatric living whitefish morphs were specialized: LSR whitefish was a littoral benthivore, small sparsely rakered whitefish was a profundal benthivore and densely rakered (DR) whitefish was a pelagic planktivore. In the lake with allopatric whitefish, zooplankton prey did not migrate vertically to avoid predation whereas, in the lake with sympatric whitefish, all important prey taxa migrated significantly. Trait utility was observed as significantly smaller size of prey in environment and predator diet in the lake with DR whitefish than in the lake with only LSR whitefish.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 561–572.