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.     

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.     

Colour plasticity and background matching in a threespine stickleback species pair

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

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.     

Evolution and assessment of colour patterns in stream-resident and anadromous male threespine stickleback Gasterosteus aculeatus from three regions

We compared the colour patterns of free swimming, reproductively active male threespine stickleback Gasterosteus aculeatus of the anadromous and stream ecotypes from three geographically distinct regions. Consistent with the hypothesis of environmentally mediated selection, our results indicate ecologically replicated differences in G. aculeatus coloration between anadromous and stream-resident populations, and that G. aculeatus probably have the visual acuity to discriminate colour pattern differences between anadromous and stream-resident fish.     

Historical and ecological correlates of body shape in the brook stickleback, Culaea inconstans

Using geometric morphometric methods, we evaluated the correlation between phenotypic variation and available historical and habitat information for two genetically differentiated, allopatric lineages of a widespread North American species, the brook stickleback ( Culaea inconstans ). The results obtained revealed strong patterns of structured phenotypic differentiation across the species range with extreme phenotypes occurring at the northwest and southeast range boundaries. Shape variation was broadly congruent with the distribution of two mitochondrial DNA lineages; a deep-bodied eastern form (Atlantic refugium) and a slim-bodied western form (Mississippian refugium); however, the two forms were not lineage-specific and phenotypic cladistic diversification is likely to be an artefact of underlying clinal variation associated with longitudinal and latitudinal gradients. In addition, we found little evidence of diagnosable lake and river forms across North America. Taken together, large-scale patterns of phenotypic diversity observed in C. inconstans suggest that relatively recent factors, such as continually varying natural selection across the range and/or potential local gene flow, may substantially mitigate the effects of historical separation or a generalized adaptive response to alternative habitats.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 769–783.     

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.     

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。     

Variable predation regimes predict the evolution of sexual dimorphism in a population of threespine stickleback

Sexual dimorphism is widespread in nature and can be influenced by sex-specific natural selection resulting from ecological differences between the sexes. Here we show that contrasting life-history pressures and temporal shifts in ecology can exert a strong influence on the evolution of sexual dimorphism. The bony spines exhibited by stickleback are a defense against open-water avian predators but may be detrimental against benthic macroinvertebrate predators. Female stickleback from a coastal lake in western Canada occupy a more open-water ecological niche and exhibit greater dorsal and pelvic spine number than males, but the magnitude of these differences varies among life-history stages, seasons, and years. Ecological data on diet and parasite load and 62 seasonal estimates of selection over a 15-year period show that selection favors increased spine number in females and decreased spine number in males, but only when pronounced ecological differences between the sexes results in differential exposure to the two, divergent predation regimes. Thus occasional sex-reversals in ecological niche reversed the mode of selection. These processes caused a predictable response in the subsequent generation, indicating that divergent predation caused evolutionary change in dimorphism. However, temporal oscillations in sex-specific selection resulted in no net change in sexual dimorphism over the 15-year study period, indicating that fluctuations in directional selection can be responsible for long-term stasis. Replicated shifts in selective regime can demonstrate the primacy of ecological processes in driving evolution and our results illustrate how such shifts are detectable using long-term monitoring of natural populations.     

Nonlinear effects of temperature on body form and developmental canalization in the threespine stickleback

Theoretical models predict that nonlinear environmental effects on the phenotype also affect developmental canalization, which in turn can influence the tempo and course of organismal evolution. Here, we used an oceanic population of threespine stickleback (Gasterosteus aculeatus) to investigate temperature‐induced phenotypic plasticity of body size and shape using a paternal half‐sibling, split‐clutch experimental design and rearing offspring under three different temperature regimes (13, 17 and 21 °C). Body size and shape of 466 stickleback individuals were assessed by a set of 53 landmarks and analysed using geometric morphometric methods. At approximately 100 days, individuals differed significantly in both size and shape across the temperature groups. However, the temperature‐induced differences between 13 and 17 °C (mainly comprising relative head and eye size) deviated considerably from those between 17 and 21 °C (involving the relative size of the ectocoracoid, the operculum and the ventral process of the pelvic girdle). Body size was largest at 17 °C. For both size and shape, phenotypic variance was significantly smaller at 17 °C than at 13 and 21 °C, indicating that development is most stable at the intermediate temperature matching the conditions encountered in the wild. Higher additive genetic variance at 13 and 21 °C indicates that the plastic response to temperature had a heritable basis. Understanding nonlinear effects of temperature on development and the underlying genetics are important for modelling evolution and for predicting outcomes of global warming, which can lead not only to shifts in average morphology but also to destabilization of development.     

Habitat‐specific trends in ontogeny of body shape in stickleback from coastal archipelago: Potential for rapid shifts in colonizing populations

We investigated ontogenetic trends in body shape of 54 freshwater (48 lake, seven stream) and six anadromous populations of threespine stickleback (Gasterosteus aculeatus L.) from the Haida Gwaii archipelago off the west coast of Canada. Multivariate analysis of covariance on the partial warp scores generated from 12 homologous landmarks on 1,958 digital images of subadult and adult male stickleback indicated that there was considerable variability of population ontogenetic slopes. We used discriminant function analysis to quantify body shape and determined that anadromous stickleback, which are ancestral to the freshwater populations, have a strongly negative ontogenetic slope (?5.62; increased streamlining with increased size). All freshwater populations exhibit a more positive slope (91% differed significantly from the marine slope), with the differences being most accentuated in populations from ponds and streams. In pristine lakes, ontogenetic slope could be predicted by lake volume as well as multivariate measures of habitat. Evidence from field transplant experiments of one of the intact populations indicates a rapid change (5 years) from allometric to isometric growth, equivalent to about half of the total slope variation among intact populations on the archipelago. We interpret this shift as developmental plasticity and suggest this may comprise the precursor for selection of optimal body shapes in these stickleback populations. J. Morphol., 2011. © 2011 Wiley‐Liss, Inc.     

Strong and parallel salinity‐induced phenotypic plasticity in one generation of threespine stickleback

Phenotypic plasticity is a major factor contributing to variation of organisms in nature, yet its evolutionary significance is insufficiently understood. One example system where plasticity might have played an important role in an adaptive radiation is the threespine stickleback (Gasterosteus aculeatus), a fish that has diversified after invading freshwater lakes repeatedly from the marine habitat. The parallel phenotypic changes that occurred in this radiation were extremely rapid. This study evaluates phenotypic plasticity in stickleback body shape in response to salinity in fish stemming from a wild freshwater population. Using a split‐clutch design, we detected surprisingly large phenotypically plastic changes in body shape after one generation. Fish raised in salt water developed shallower bodies and longer jaws, and these changes were consistent and parallel across families. Although this work highlights the effect of phenotypic plasticity, we also find indications that constraints may play a role in biasing the direction of possible phenotypic change. The slopes of the allometric relationship of individual linear traits did not change across treatments, indicating that plastic change does not affect the covariation of traits with overall size. We conclude that stickleback have a large capacity for plastic phenotypic change in response to salinity and that plasticity and evolutionary constraints have likely contributed to the phenotypic diversification of these fish.     

Adaptation and constraint in a stickleback radiation

The evolution of threespine sticklebacks in freshwater lakes constitutes a well‐studied example of a phenotypic radiation that has produced numerous instances of parallel evolution, but the exact selective agents that drive these changes are not yet fully understood. We present a comparative study across 74 freshwater populations of threespine stickleback in Norway to test whether evolutionary changes in stickleback morphology are consistent with adaptations to physical parameters such as lake depth, lake area, lake perimeter and shoreline complexity, variables thought to reflect different habitats and feeding niches. Only weak indications of adaptation were found. Instead, populations seem to have diversified in phenotypic directions consistent with allometric scaling relationships. This indicates that evolutionary constraints may have played a role in structuring phenotypic variation across freshwater populations of stickleback. We also tested whether the number of lateral plates evolved in response to lake calcium levels, but found no evidence for this hypothesis.     

Ecological and evolutionary factors in the morphological diversification of South American spiny rats

Understanding the processes underlying morphological diversification is a central goal in ecology and evolutionary biology and requires the integration of information about phylogenetic divergence and ecological niche diversity. In the present study, we use geometric morphometrics and comparative methods to investigate morphological diversification in Neotropical spiny rats of the family Echimyidae. Morphological diversification is studied as shape variation in the skull, comprising a structure composed of four distinct units: vault, base, orognathofacial complex, and mandible. We demonstrate association among patterns of variation in shape in different cranial units, levels of phylogenetic divergence, and ecological niche diversification. At the lower level of phylogenetic divergence, there is significant and positive concordance between patterns of phylogenetic divergence and cranial shape variation in all cranial units. This concordance may be attributable to the phylogenetic and shape distances being calculated between species that occupy the same niche. At higher phylogenetic levels of divergence and with ecological niche diversity, there is significant concordance between shape variation in all four cranial units and the ecological niches. In particular, the orognathofacial complex revealed the most significant association between shape variation and ecological niche diversity. This association may be explained by the great functional importance of the orognathofacial complex.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 646–660.     

How feeding performance and energy intake change with a small increase in the body size of the three-spined stickleback

Changes in the foraging behaviour due to variation in the body size of the three-spined stickleback Gasterosteus aculeatus were investigated. All sizes of fish had a high probability of attacking prey whenever encountered. The probability of eating the prey increased with the size of the fish, as the larger fish had larger jaws and a greater stomach capacity. Therefore, as fish increased in size there was an increase in the probability of successful prey capture. The level of satiation did not have an effect on the prey handling time, which is contrary to other studies and is probably a result of the large prey sizes. The physical size of the prey meant that the handling times were long regardless of the motivational level of the fish. The larger fish took in more energy and at a faster rate, although the time to reach satiation was similar for all fish sizes. The advantage that large fish appear to have in successfully gaining large prey is negated by their greater metabolic requirement. The changes in feeding performance induced by small increases in body size could have important consequences for intraspecific competition, habitat Use and risk of predation.     

10 000 years later: evolution of body shape in Haida Gwaii three-spined stickleback

The body shape of 1303 adult male three-spined stickleback Gasterosteus aculeatus from 118 populations on Haida Gwaii archipelago off the mid-coast of British Columbia was investigated using discriminant function analysis on partial warp scores generated from 12 homologous landmarks on a digital image of each fish. Results demonstrated geographical differences in adult body shape that could be predicted by both abiotic and biotic factors of the habitat. Populations with derived shape (CV1−), including thick peduncles, posterior and closely spaced dorsal spines, anterior pelvis, small dorsal and anal fins, were found in small, shallow, stained ponds, and populations with less derived shape (CV1+), with small narrow peduncles, anterior and widely spaced dorsal spines, posterior pelvis, large dorsal and anal fins were found in large, deep, clear lakes. This relationship was replicated between geographic regions; divergent mtDNA haplotypes in lowland populations; between predation regimes throughout the archipelago, and in each geographical region and between predation regimes in lowland populations monomorphic for the Euro and North American mtDNA haplotype. There were large-bodied populations with derived shape (CV2−), including small heads and shallow elongate bodies in open water habitats of low productivity, and populations with smaller size and less derived shape (CV2+), with large heads and deeper bodies in higher productivity, structurally complex habitats. This relationship was replicated between geographic regions, and partially between divergent mtDNA haplotypes in lowland populations. Field tests for phenotypic plasticity of body shape suggest that <10% of the total variation in body shape among populations throughout the archipelago can be attributed to plasticity.     

Contrasting patterns of body shape and neutral genetic divergence in marine and lake populations of threespine sticklebacks

Comparisons of neutral marker and quantitative trait divergence can provide important insights into the relative roles of natural selection and neutral genetic drift in population differentiation. We investigated phenotypic and genetic differentiation among Fennoscandian threespine stickleback (Gasterosteus aculeatus) populations, and found that the highest degree of differentiation occurred between sea and freshwater habitats. Within habitats, morphological divergence was highest among the different freshwater populations. Pairwise phenotypic and neutral genetic distances among populations were positively correlated, suggesting that genetic drift may have contributed to the morphological differentiation among habitats. On the other hand, the degree of phenotypic differentiation (PST) clearly surpassed the neutral expectation set by FST, suggesting a predominant role for natural selection over genetic drift as an explanation for the observed differentiation. However, separate PST/FST comparisons by habitats revealed that body shape divergence between lake and marine populations, and even among marine populations, can be strongly influenced by natural selection. On the other hand, genetic drift can play an important role in the differentiation among lake populations.     

Quantitative genetic inheritance of morphological divergence in a lake-stream stickleback ecotype pair: implications for reproductive isolation

Ecological selection against hybrids between populations occupying different habitats might be an important component of reproductive isolation during the initial stages of speciation. The strength and directionality of this barrier to gene flow depends on the genetic architecture underlying divergence in ecologically relevant phenotypes. We here present line cross analyses of inheritance for two key foraging-related morphological traits involved in adaptive divergence between stickleback ecotypes residing parapatrically in lake and stream habitats within the Misty Lake watershed (Vancouver Island, Canada). One main finding is the striking genetic dominance of the lake phenotype for body depth. Selection associated with this phenotype against first- and later-generation hybrids should therefore be asymmetric, hindering introgression from the lake to the stream population but not vice versa. Another main finding is that divergence in gill raker number is inherited additively and should therefore contribute symmetrically to reproductive isolation. Our study suggests that traits involved in adaptation might contribute to reproductive isolation qualitatively differently, depending on their mode of inheritance.     

Rapid genetic divergence in postglacial populations of threespine stickleback (Gasterosteus aculeatus): the role of habitat type, drainage and geographical proximity

The goal of this study was to evaluate the role of common ancestry, and of geographical or reproductive isolation, in genetic divergence in populations of threespine sticklebacks (Gasterosteus aculeatus). Using seven DNA microsatellite loci we compared the effects of habitat type, drainage system and geographical proximity on genetic distance among 16 populations situated in an area in Schleswig-Holstein (Germany) that became deglaciated approximately 12 000 years ago. Stickleback population structure correlated only weakly with drainage system, whereas the primary divergence was among habitat types. Phylogenetic analysis revealed that lake (n = 7) and river (n = 5) populations formed two distinct clades (Cavalli-Sforza's and Edwards' chord distance, 82-100% bootstrap support) at approximately equal genetic distances to a third clade, comprising putative estuarine (n = 4) ancestors. Allele frequencies in lake and river populations represented different subsets of the genetically more diverse estuarine populations. In nested amovas approximately twice the genetic variance was distributed among lake vs. river vs. estuarine populations as compared with the combined effects of drainage system and geographical distance. Limited gene flow between habitat types must have been established after postglacial colonization, suggesting ecological hybrid inferiority or behavioural mating barriers between ecotypes. Within estuarine and lake populations, population differentiation followed an isolation-by-distance model. Given the high observed heterozygosities within the 16 study populations (HO = 0.65-0.87), the mean divergence between lake and river population pairs (FST = 0.18 +/- 0.007) would be reached after 300-6000 generations in a stepwise mutation model, depending on the size of N(e). This demonstrates both the utility of hypervariable microsatellites for detecting recent population divergences and the danger of operating at temporal or spatial scales which are beyond their resolution.