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.     

Morphological segregation of Icelandic threespine stickleback (Gasterosteus aculeatus L).

Icelandic threespine sticklebacks show parallel sympatric morphological differences related to different substrate habitats in four Icelandic lakes. The level of morphological diversification varies among the lakes, ranging from a population with a wide morphological distribution to a population with clear resource morphs, where morphological diversification was reflected in diet differences. These differences in morphological divergence are closely related to the differences in the ecological surroundings of each population. This appears to be resource polymorphism, which may lead to population differentiation and speciation. Trophically related sexual dimorphism was also common in these sticklebacks, which is possibly the result of sexual selection or habitat segregation by the sexes. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 76 , 247–257.     

Phenotypic divergence and reproductive isolation between sympatric forms of Japanese threespine sticklebacks

The threespine stickleback ( Gasterosteus aculeatus ) species complex is well suited for identifying the types of phenotypic divergence and isolating barriers that contribute to reproductive isolation at early stages of speciation. In the present study, we characterize the patterns of genetic and phenotypic divergence as well as the types of isolating barriers that are present between two sympatric pairs of threespine sticklebacks in Hokkaido, Japan. One sympatric pair consists of an anadromous and a resident freshwater form and shows divergence in body size between the forms, despite the lack of genetic differentiation between them. The second sympatric pair consists of two anadromous forms, which originated before the last glacial period and are currently reproductively isolated. These two anadromous forms have diverged in many morphological traits as well as in their reproductive behaviours. Both sexual isolation and hybrid male sterility contribute to reproductive isolation between the anadromous species pair. We discuss the shared and unique aspects of phenotypic divergence and reproductive isolation in the Japanese sympatric pairs compared with postglacial stickleback species pairs. Further studies of these divergent species pairs will provide a deeper understanding of the mechanisms of speciation in sticklebacks.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 671–685.     

Differential predation on the two colour morphs of Nicaraguan Crater lake Midas cichlid fish: implications for the maintenance of its gold‐dark polymorphism

Predation can play an important role in the evolution and maintenance of prey colour polymorphisms. Several factors are known to affect predator choice, including the prey's relative abundance and conspicuousness. In polymorphic prey species, predators often target the most common or most visible morphs. To test if predator choice can explain why in Midas cichlid fish the more visible (gold) morph is also more rare than the inconspicuous dark morph, we conducted predation experiments using two differently coloured wax models in Nicaraguan crater lakes. Contrary to expectations, we observed an overall higher attack rate on the much more abundant, yet less conspicuous dark models, and propose frequency‐dependent predation as a potential explanation for this result. Interestingly, the attack rate differed between different types of predators. While avian predators were biased towards the abundant and less colourful dark morphs, fish predators did not show a strong bias. However, the relative attack rate of fish predators seemed to vary with the clarity of the water, as attack rates on gold models went up as water clarity decreased. The relative differential predation rates on different morphs might impact the relative abundance of both colour morphs and thus explain the maintenance of the colour polymorphism. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112 , 123–131.     

The interplay between multiple predators and prey colour divergence

Evolutionary divergence in the coloration of toxic prey is expected when geographic variation in predator composition and behavior favours shifts in prey conspicuousness. A fundamental prediction of predator‐driven colour divergence is that the local coloration should experience lower predation risk than novel prey phenotypes. The dorsal coloration of the granular poison frog varies gradually from populations of conspicuous bright red frogs to populations of dull green and relatively cryptic frogs. We conducted experiments with clay models in four populations to examine the geographic patterns of taxon‐specific predation. Birds avoided the local phenotype while lizards consistently selected for decreased conspicuousness and crab predation did not depend on frog coloration. Importantly, birds and lizards favoured low conspicuousness in populations where relatively cryptic green morphs have evolved. This study provides evidence for the interplay among distinct selective pressures, from multiple‐predator taxa, acting on the divergence in protective coloration of prey species. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 580–589.     

Effects of population,family, and diet on craniofacial morphology of Icelandic Arctic charr (Salvelinus alpinus)

We evaluated hypotheses of intralacustrine diversification and plastic responses to two diet environments in Icelandic Arctic charr (Salvelinus alpinus). Full‐sib families of progeny of wild polymorphic charr from two lakes where morphs vary in their degree of phenotypic and ecological divergence were split, with half of the offspring reared on a benthic and half on a limnetic type of diet to estimate family norms of reaction. We focused on variation in craniofacial traits because they are probably functionally related to diet and complement a previous study of body shape in these charr. A hierarchical analysis of phenotypic variation between lakes, pairs of morphs within each lake, and two families within each morph found that phenotypic variation partitioned between families relative to morphs was reduced in the more ecologically diversified population, which is consistent with adaptive diversification. The effect size of plastic responses between lake populations was similar, suggesting little difference in the degree of canalization in contrast to a previous analysis of body form plasticity. Thus, the role that plastic morphological responses play in the adaptive diversification of morphs and different lake populations of Arctic charr may depend on the trait. © 2013 The Linnean Society of London     

Morphological and genetic analysis of fish of a Carassius complex (Cyprinidae) in Lake Kasumigaura with reference to the taxonomic status of two all-female triploid morphs

The classification of the Carassius complex (Cyprinidae) including all-female triploids, called ginbuna in Japanese, is so confused that three sympatric morphs of crucian carp in Lake Kasumigaura are categorized into two different subspecies within a species. We examined them in order to explain the coexistence of more than one subspecies and determine the founder of the triploid lineages in the crucian carp fauna in the lake. Principal component analysis proved that the three sympatric morphs had a morphometric basis distinguishable from each other. Ploidy was determined by flow cytometry which showed triploids in two morphs and diploids in the other morph. Stepwise discriminant analysis using only meristic characteristics could separate the diploids from the triploids. Phylogenetic analysis using mitochondrial DNA inferred two lineages in which one was composed of a triploid morph and the other was a diploid–triploid mixture. Disagreement between the taxonomic status and the phylogenetic status is explicable by assuming that the triploids in the Carassius complex had independent origins leading to the different subspecies. C. auratus langsdorfii appears to show genetic complexities that traditional taxonomic classification can not unravel.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 79 , 351–357.     

Positive assortative mating between recently described sympatric morphs of Icelandic sticklebacks

Recently, models of sympatric speciation have suggested that assortative mating can develop between sympatric morphs due to divergence in an ecologically important character. For example, in sympatric pairs of threespine stickleback (Gasterosteus aculeatus L.) size-assortative mating seems to be instrumental in reproductive isolation. Here, we examine courtship behaviour and assortative mating of newly described sympatric stickleback morphs in Lake Thingvallavatn, Iceland. We find that the two morphs show strong positive assortative mating. However, the mechanism involved in mate choice does not seem to be as straightforward as in other similar systems of sympatric stickleback morphs and may involve variation in nest type.     

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.     

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, ?? , ??–??.     

One cost of being gold: selective predation and implications for the maintenance of the Midas cichlid colour polymorphism (Perciformes: Cichlidae)

In the colour‐polymorphic Midas cichlid fish species complex (Amphilophus citrinellus spp.), gold morphs occur at much lower frequencies (< 10%) than dark individuals. This might be surprising because gold coloration is dominant and coded for by a single Mendelian locus. Furthermore, gold individuals are considered to be competitively advantaged over dark ones because they grow faster and win aggressive encounters more often compared to dark individuals of equal size. However, one might expect a cost of being gold in terms of natural selection as a result of predation. We tested whether the Jaguar cichlid (Parachromis managuensis), a major fish predator of Midas cichlids, preys differentially on colour variants of goldfish (Carassius auratus auratus), which were used as a proxy for Midas cichlids because of their similarity in colour. Size‐matched pairs of prey fish (gold and dark) were offered to the predator and the time until the fish were attacked was recorded. The gold morph was attacked first more often (approximately 70%) but not faster than the dark morph. This suggests that the predator perceives the gold individual first, and/or that the predator exhibits a preference or higher motivation to attack the gold prey fish. The increased risk of predation of gold prey fish suggests for the Midas cichlid system that being gold may carry significant costs in terms of natural selection as a result of its major piscivorous predator. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 350–358.     

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.     

Evidence for asymmetric migration load in a pair of ecologically divergent stickleback populations

Gene flow between ecologically divergent populations can prevent local adaptation, resulting in lower mean fitness and directional selection within a population. Such maladaptation should tend to be stronger in populations receiving a relatively larger fraction of immigrants. We test this expectation by comparing the strength of selection in a pair of three-spine stickleback populations in adjoining but unequal-sized lake basins in British Columbia. A larger deeper basin is connected to a smaller shallower basin by a short channel that allows extensive migration between populations. The two basins contain distinct habitats and prey communities, and stickleback stomach contents and isotope ratios differ accordingly. Trophic morphology is correlated with diet, so we would expect these ecological differences to be accompanied by morphological divergence. However, high gene flow appears to constrain adaptive divergence: microsatellites indicate that the two basins represent a single panmictic gene pool, and phenotypic divergence is very subtle. As a result, fish in the smaller lake basin are subject to persistent directional selection towards a more benthic phenotype, whereas the larger population exhibits no significant selection. The results illustrate the potentially asymmetrical effect of migration-selection balance, and its effect on fitness within populations.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 273–287.     

Habitat-associated morphological divergence in two Neotropical fish species

We examined intraspecific morphological diversification between river channel and lagoon habitats for two Neotropical fish ( Bryconops caudomaculatus , Characidae; Biotodoma wavrini , Cichlidae). We hypothesized that differences between habitats (e.g. flow regime, foraging opportunities) might create selective pressures resulting in morphological divergence between conspecific populations. We collected fish from four channel-lagoon habitat pairs in the Río Cinaruco, Venezuela, and compared body morphology using geometric morphometrics. There were two aspects of divergence in both species: (1) placement of maximum body depth and (2) orientation of the mouth. For both species, maximum body depth was positioned more anteriorly (i.e. fusiform) in the river channel than in lagoons. Both species exhibited a relatively terminal mouth in lagoons compared to the channel. The mouth of B. caudomaculatus was relatively upturned, whereas the mouth of B. wavrini was relatively subterminal, in channel habitats. Observed morphological patterns are consistent with functional morphological principles suggesting adaptive divergence. We also show that spatial distance between habitats, presumably reflecting rates of population mixing, appears to have constrained diversification. For both species, morphological divergence increased with distance between habitats. Thus morphological divergence between channel and lagoon habitats apparently reflects a balance between diversification driven by natural selection, and homogenization driven by population mixing.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 80 , 689–698.     

Colonization of novel White Sands habitat is associated with changes in lizard anti‐predator behaviour

Colonization of novel habitats is often associated with differences in ecological community composition. For small diurnal animals, differences in predator diversity and abundance can lead to behavioural shifts in the novel habitat. The eastern fence lizard Sceloporus undulatus (Bosc and Daudin, 1801) recently colonized the gypsum dunes of White Sands, a predator‐poor community relative to the predator‐rich community of the surrounding Chihuahuan dark‐soil habitat. We used field experiments to assess S. undulatus anti‐predator behaviour in white‐sand versus dark‐soil habitats, and used laboratory assays to determine whether behavioural differences could be mediated by hormonal regulation. Overall, we found that white‐sand lizards were less vigilant but more wary than their dark‐soil counterparts; it took them longer to detect a simulated predator, but once detected they were more likely to retreat from their perches than dark‐soil lizards. At the proximate level, differences in anti‐predator behaviour could not be explained by differences in plasma hormone levels (corticosterone and testosterone); we detected elevated corticosterone for lizards in our stress treatment relative to control treatment, but found no differences between habitats in baseline or acute corticosterone levels. At the evolutionary level, we suggest that differences in anti‐predator behaviour may be explained by differences across habitats in predation environment, habituation, and/or the cost of retreating. Our study implicates changes in predator community composition in mediating ecological divergence in behaviour. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 657–667.     

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.     

Divergence in social foraging among morphs of the three‐spined stickleback,Gasterosteus aculeatus

Foraging in social groups has a number of benefits but can also increase the risk of exploitation. High tendency to shoal may be correlated with groups foraging, although facultatively social fish adjust both shoaling decisions and food resource defence based on intrinsic and extrinsic factors. The main aim of this study was to examine the relationships between shoaling, solitary foraging and aggression, forager tolerance of conspecifics joining at a discovered food patch and forager exploitation of resources discovered by others. We used two intra‐lacustrine three‐spined stickleback morph pairs, lava and mud, and monomorphic morphs from each of lava and mud habitats. The lava morph formed less cohesive shoals, was bolder during solitary foraging, approached and entered an occupied food patch less frequently than the mud morph, suggesting a link between shoaling and the propensity for social foraging. However, shoaling tendency and joiner tolerance were not correlated at a population level. Intralacustrine lava and mud morphs differed more markedly in joiner tolerance than morphs from single habitat lakes, whereas the opposite was true for shoaling tendency. We conclude that, in addition to differentiation in shoaling tendency, the lava and mud morphs differ in social foraging and these variations may act to promote population divergence. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 194–203.     

Morphological anti‐predator defences in the nine‐spined stickleback: constitutive,induced or both?

Environmental differences among populations are expected to lead to local adaptation, while spatial or temporal environmental variation within a population will favour evolution of phenotypic plasticity. As plasticity itself can be under selection, locally adapted populations can vary in levels of plasticity. Nine‐spined stickleback (Pungitius pungitius) originating from isolated ponds (low piscine predation risk, high competition) vs. lake and marine populations (high piscine predation risk, low competition) are known to be morphologically adapted to their respective environments. However, nothing is known about their ability to express phenotypic plasticity in morphology in response to perceived predation risk or food availability/competition. We studied predator‐induced phenotypic plasticity in body shape and armour of marine and pond nine‐spined stickleback in a factorial common garden experiment with two predator treatments (present vs. absent) and two feeding regimes (low vs. high). The predation treatment did not induce any morphological shifts in fish from either habitat or food regime. However, strong habitat‐dependent differences between populations as well as strong sexual dimorphism in both body shape and armour were found. The lack of predator‐induced plasticity in development of the defence traits (viz. body armour and body depth) suggests that morphological anti‐predator traits in nine‐spined stickleback are strictly constitutive, rather than inducible. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ??, ??–??.     

Extreme habitats are not refuges: poeciliids suffer from increased aerial predation risk in sulphidic southern Mexican habitats

Extreme environments are often considered a predation refuge for organisms living in them. In southern Mexico several species of poeciliid fishes are undergoing incipient speciation in a variety of extreme (i.e. permanently dark and/or sulphidic) freshwater systems, and previous research has demonstrated reproductive isolation between populations from sulphidic and adjacent benign habitats. In the present study, we investigated bird predation rates (measured as successful captures per minute) in two sulphidic surface and several benign surface habitats, to test the hypothesis that extreme habitats are predation refuges. We found capture rates to be approximately 20 times higher in sulphidic environments: probably facilitated by extremophile poeciliids spending most of their time at the water surface, where they engage in aquatic surface respiration as a direct response to hypoxia. Even birds that are usually not considered major fish predators regularly engage in fish predation in the toxic habitats of southern Mexico. Our results demonstrate that extreme environments do not necessarily represent a refuge from predation, and we discuss the general importance of predation in driving incipient speciation in these systems. Finally, we hypothesize that natural selection via avian predation may play an important role in maintaining reproductive isolation between divergent poeciliid populations. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 417–426.     

Molecular genetic examination of the polymorphic Arctic charr Salvelinus alpinus of Thingvallavatn, Iceland

Thingvallavatn, Iceland contains two sympatric morphotypes (benthic and limnetic) of Arctic charr Salvelinus alpinus. Each morphotype is composed of two morphs and these differ markedly in ecology, behaviour and life history. We used molecular genetic approaches to test whether (i) genetic heterogeneity exists among morphs and (ii) if morphs arose in allopatry and came into secondary contact or arose sympatrically within the lake through genetic segregation and/or phenotypic plasticity. Direct sequencing of 275 bp of the mitochondrial DNA (mtDNA) control region, mtDNA restriction fragment length polymorphisms and single locus minisatellite analyses detected insufficient variation to test our hypotheses. Analysis of multilocus minisatellite band sharing detected no significant differences between morphs within the same morphotype. However, significant differences among morphs belonging to different morphotypes suggest some genetic heterogeneity in Thingvallavatn charr. Limnetic charr from Thingvallavatn were more similar to sympatric benthic charr than to allopatric limnetics from two other Icelandic lakes. This suggests that the Thingvallavatn morphs arose sympatrically within the lake rather than in allopatry followed by secondary contact.