Genetic and morphological divergence along the littoral–pelagic axis in two common and sympatric fishes: perch,Perca fluviatilis (Percidae) and roach,Rutilus rutilus (Cyprinidae)

Individuals are constantly in competition with one another and, on both ecological and evolutionary timescales, processes act to reduce this competition and promote the gain of fitness advantages via diversification. Here we have investigated the genetic (AFLP) and morphological (geometric morphometrics) aspects of the littoral–pelagic axis, a commonly observed resource polymorphism in freshwater fishes of postglacial lakes. We found a large degree of variation in the genetic and morphological divergence between littoral and pelagic perch and roach across Swedish lakes. Although there was evidence of assortative mating (elevated kinship values) in both species, we could not find any significant coupling of morphology and genetic divergence. Instead, there was evidence that the extent of resource polymorphism may be largely caused by phenotypic plasticity. These results suggest that assortative mating, which can lead to genetically determined adaptive divergence, does occur in these species, particularly perch, but not according to genetically fixed morphological traits. The behavioural mechanisms facilitating associative mating need to be investigated to explore the interaction between phenotypic plasticity and adaptive genetic divergence and their roles in diversification. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 929–940.     

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     

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.     

Testing the role of coadapted genes versus bet-hedging for mating strategies in colour polymorphic pygmy grasshoppers

Recent investigations of mate choice indicate that the genetic effect of sires on offspring fitness may depend on the interaction between maternal and paternal genotypes and the environmental conditions experienced by the offspring. Alternative colour morphs of the pygmy grasshopper, Tetrix subulata , represent ecological strategies that differ in body size, life history, thermoregulatory behaviour, and habitat selection. The hypothesis that selection promotes behaviours maintaining coadapted gene complexes predicts individuals to mate assortatively with respect to colour morph. On the other hand, the bet-hedging hypothesis predicts that the temporal variability of the environment inhabited by these animals may select for disassortative mating behaviour resulting in heterogeneous offspring. To distinguish between these competing hypotheses, we investigated mating behaviours using dual-choice experiments. Our results were not in agreement with the prediction of assortative mating but suggest instead that matings were random with regard to colour morph. Polyandry was common, and females mated with the second male regardless of whether the first mating was assortative or disassortative. Polyandry also was equally frequent among females in triads in which the two males belonged to different colour morphs as in triads where both males belonged to the same colour morph. A field experiment confirmed that polyandry occurred also among free-ranging individuals, and uncovered variation in mating success among male colour morphs, probably due to indirect effects of coloration on activity or habitat use. The consequences of this random and polyandrous mating strategy for the evolutionary dynamics of the colour polymorphism remain to be explored.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 491–499.     

Assortative mating counteracts the evolution of dispersal polymorphisms

Polymorphic dispersal strategies are found in many plant and animal species. An important question is how the genetic variation underlying such polymorphisms is maintained. Numerous mechanisms have been discussed, including kin competition or frequency-dependent selection. In the context of sympatric speciation events, genetic and phenotypic variation is often assumed to be preserved by assortative mating. Thus, recently, this has been advocated as a possible mechanism leading to the evolution of dispersal polymorphisms. Here, we examine the role of assortative mating for the evolution of trade-off-driven dispersal polymorphisms by modeling univoltine insect species in a metapopulation. We show that assortative mating does not favor the evolution of polymorphisms. On the contrary, assortative mating favors the evolution of an intermediate dispersal type and a uni-modal distribution of traits within populations. As an alternative, mechanism dominance may explain the occurrence of two discrete morphs.     

Revealing the mechanisms of sexual isolation in a case of sympatric and parallel ecological divergence

Two ecotypes of a marine intertidal snail (Littorina saxatilis), living at different microhabitats and shore levels, have evolved in sympatry and in parallel across the Galician rocky shore. These ecotypes differ in many traits (including size) due to differential adaptation. They meet, mate assortatively, and partially hybridize at the mid shore where the two microhabitats overlap. The partial sexual isolation observed is claimed to be a side‐effect of the size differences between ecotypes combined with a size assortative mating found in most populations of this species. We investigated this hypothesis using three complementary experimental approaches. First, we investigated which of the different shell variables contributed most to the variation in individual sexual isolation in the field by using two new statistics developed for that purpose: (1) pair sexual isolation and (2) r_i, which is based on the Pearson correlation coefficient. We found that size is the most important trait explaining the sexual isolation and, in particular, the males appear to be the key sex contributing to sexual isolation. Second, we compared the size assortative mating between regions: exposed rocky shore populations from north‐westwern Spain (showing incomplete reproductive isolation due to size assortative mating) and protected Spanish and Swedish populations (showing size assortative mating but not reproductive isolation between ecomorphs). Most of the variation in size assortative mating between localities was significantly explained by the within‐population level of variation on size. Third, we performed a laboratory male choice experiment, which further suggested that the choice is made predominantly on the basis of size. These results confirm the mechanism proposed to explain the sexual isolation in the Galician hybrid zone and thus support this case as a putative example of parallel incipient speciation. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 94 , 513–526.     

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.     

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.     

Resource polymorphism in a Patagonian fish Percichthys trucha (Percichthyidae): phenotypic evidence for interlake pattern variation

Within-species differentiation in phenotypic characters related to resource use (resource polymorphism) is frequently thought to result from divergent natural selection in a heterogeneous environment with 'open niches'. In this study we found consistent resource-based polymorphism within three different populations of Percichthys trucha , a lake-dwelling fish native to the southern Andes. In each of three lakes we found two morphotypes that could be clearly distinguished by differences in gill raker length. However, the magnitude of the polymorphism, and the suite of phenotypic characteristics associated with the polymorphism, differed between lakes. Patterns of divergence were more similar between the two northern lakes which ultimately drain into a common river, than between these two lakes and a more southern, unconnected lake. The southern population, which had the largest divergence in gill raker length (32% vs. 16% and 19%), also showed substantial differences in diet. Evidence from the southern population suggests that polymorphism in P. trucha is present early during ontogeny. We conclude that while there are some strong parallels among lakes in the development of a trophic polymorphism, differences in environmental ­conditions and/or colonization history have led to substantial differences in the evolutionary history, resulting in ­different ecological roles of common morphotypes within different lakes.  © 2003 The Linnean Society of London . Biological Journal of the Linnean Society , 2003, 78 , 497–515.     

Ecosystem size matters: the dimensionality of intralacustrine diversification in Icelandic stickleback is predicted by lake size

Cases of evolutionary diversification can be characterized along a continuum from weak to strong genetic and phenotypic differentiation. Several factors may facilitate or constrain the differentiation process. Comparative analyses of replicates of the same taxon at different stages of differentiation can be useful to identify these factors. We estimated the number of distinct phenotypic groups in three‐spine stickleback populations from nine lakes in Iceland and in one marine population. Using the inferred number of phenotypic groups in each lake, genetic divergence from the marine population, and physical lake and landscape variables, we tested whether ecosystem size, approximated by lake size and depth, or isolation from the ancestral marine gene pool predicts the occurrence and the extent of phenotypic and genetic diversification within lakes. We find intralacustrine phenotypic diversification to be the rule rather than the exception, occurring in all but the youngest lake population and being manifest in ecologically important phenotypic traits. Neutral genetic data further indicate nonrandom mating in four of nine studied lakes, and restricted gene flow between sympatric phenotypic groups in two. Although neither the phenotypic variation nor the number of intralacustrine phenotypic groups was associated with any of our environmental variables, the number of phenotypic traits that were differentiated was significantly positively related to lake size, and evidence for restricted gene flow between sympatric phenotypic groups was only found in the largest lakes where trait specific phenotypic differentiation was highest.     

Ontogenetic shifts in phenotype–environment associations in Nile perch,Lates niloticus (Perciformes: Latidae) from Lake Nabugabo,Uganda

Habitat‐associated trait divergence may vary across ontogeny if there are strong size‐related shifts in selection pressures. We quantified patterns of phenotypic divergence in Nile perch (Lates niloticus) from ecologically distinct wetland edge and forest edge habitats in Lake Nabugabo, Uganda, and we compared patterns of divergence across three size classes to determine whether trends are consistent through Nile perch ontogeny. We predicted that inter‐habitat variation in biotic (e.g. vegetation structure) and abiotic (e.g. dissolved oxygen concentration) variables may create divergent selective regimes. We compared body morphology using geometric morphometrics and found substantial differences between habitats, although not all trends were consistent across size classes. The most striking aspects of divergence in small Nile perch were in mouth orientation, head size, and development of the caudal region. Medium‐sized Nile perch also showed differences in mouth orientation. Differences in large individuals were related to eye size and orientation, as well as caudal length. The observed patterns of divergence are consistent with functional morphological predictions for fish across divergent trophic regimes, high and low predation environments, and complex and simple habitats. Although this suggests adaptive divergence, the source of phenotypic variation is unknown and may reflect phenotypic plasticity and/or genetic differences. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 449–465.     

Transitions in cuticular composition across a hybrid zone: historical accident or environmental adaptation?

Two subspecies of the grasshopper Chorthippus parallelus form a hybrid zone in the Pyrenees. Transitions across the zone, including changes in mating signals and reproductive isolation have been intensively studied. Cuticular pheromones have been identified as likely mate recognition signals. Since the major role of the cuticle is in waterproofing, environmental adaptation of cuticular composition has the interesting potential to generate assortative mating as an incidental by-product. We describe the pattern of variation in cuticular hydrocarbon blend in four transects through the hybrid zone. We find no evidence for a previously observed displaced cline in one blend component. There were differences between subspecies but these varied among transects and were small compared with variation between transects. We examined environmental variation within one transect and found a correlation between vegetation and cuticular composition, suggesting that environment influences the constitution of the cuticle, and hence natural selection may interact with mating signals in this species.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 78 , 193−201.     

PARTITIONING THE EFFECTS OF SPATIAL ISOLATION,NEST HABITAT,AND INDIVIDUAL DIET IN CAUSING ASSORTATIVE MATING WITHIN A POPULATION OF THREESPINE STICKLEBACK

Assortative mating is measured as a phenotypic or genotypic correlation between mates. Although biologists typically view assortative mating in terms of mate preference for similar partners, correlations between mates can also arise from phenotypic spatial structure arising from spatial isolation or habitat preferences. Here, we test whether diet‐assortative mating within an ecologically variable population of threespine stickleback results from small‐scale geographic isolation or microhabitat preference. We find evidence for assortative mating in the form of a positive correlation between mated pairs’ diets (measured using stable isotopes). Stable isotopes reveal diet differences between different nesting areas and among individuals using different nest habitat within a nesting area. This spatial segregation of diet types should generate some assortative mating, but is insufficient to explain the observed assortment strength. Significant male–female isotope correlations remain after controlling for spatial variables. We therefore conclude that sticklebacks’ diet‐assortative mating arises from additional behavioral preference. More generally, our results illustrate the point that spatial segregation can only drive appreciable levels of phenotypic assortative mating when environment‐phenotype correlations are parallel and strong in both sexes. Consequently, intraspecific assortative mating may typically entail mating preferences rather than just spatial cosegregation of phenotypes.     

Population dynamics and harvesting of semelparous species with phenotypic and genotypic variability in reproductive age

We study the evolution of polymorphic life histories in anadromous semelparous salmon and the effects of harvesting. We derive dynamic phenotypic and genetic ESS models for describing the evolutionary dynamics. We show in our deterministic analysis that polymorphisms are not possible in a panmictic random mating population. Instead, genetic or behavioral polymorphisms may be observed in populations with assortative mating systems. Positive assortative mating may be supported and generated by behavioral and phenotypic traits like male mate choice, spawning ground selection by phenotype, or within-river homing-migration-distance by size. In the case of an evolutionarily stable dimorphism, the ESS is characterized by a reproductive ideal free distribution such that at an equilibrium the individuals are indifferent from the fitness point of view between the two life histories of early and late reproduction. Different strategy models - that is, phenotypic and genetic ESS models - yield identical behavioral predictions and, consequently, genetics does not seem to play an important role in the present model. An evolutionary response to increased fishing mortality is obvious and may have resource management implications. High sea fishing mortalities drive the populations toward early spawning. Thus it is possible that unselective harvesting at sea may eliminate, depending on the biological system, behavioral polymorphisms or genetic heterozygozity and drive the population to a monomorphic one. If within-river homing migration distances depend on the size of fish, unselective harvesting at sea, or selective harvesting of spawning runs in rivers, may reduce local population sizes on spawning grounds high up rivers. Finally, harvesting in a population may cause a switch in a dominant life-history strategy in a population so that anticipated sustainable yields cannot be realized in practice.     

Incipient speciation driven by phenotypic plasticity? Evidence from sympatric populations of Arctic charr

Recent models suggest that the existence of environmentally induced polymorphisms within a single population (especially those related to foraging) facilitates the process of evolutionary divergence within a single gene pool by generating distinct phenotypic modes that are exposed to differential selection. In order to test a prediction of the phenotypic plasticity model of divergence, we used a well-documented polymorphism to disentangle the relative effects of morph and rearing environment in generating phenotypic variance. We reared first-generation offspring of two sympatric morphs of Arctic charr Salvelinus alpinus in the laboratory and compared their head morphology with that of their wild parents. Morphological characters with a known functional role in foraging were highly plastic. Rearing environment accounted for the largest component of the variation in expressed phenotype, but this environmental effect overlaid a clear (but small) genetic effect. We conclude that phenotypic plasticity has played a significant role in the evolution of this trophic polymorphism, but that the evolutionary process has progressed to the point that the gene pool is now segregated.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 81 , 611–618.     

On the role of sexual selection in ecological divergence: a test of body‐size assortative mating in the eastern newt Notophthalmus viridescens

Speciation processes initiated by divergent selection often fail to complete; yet, how sexual selection is involved in the progress of ecological speciation is rarely understood. Intraspecific body‐size variation affects mate preference and male–male competition, which can consequently lead to assortative mating based on body size. In the present study, we tested the importance of body size difference in the potential of assortative mating between the two eastern newt subspecies, larger Notophthalmus viridescens viridescens and smaller Notophthalmus viridescens dorsalis. Through differential expression of life‐cycle polyphenism, these two subspecies are adapted to contrasting environments, which has likely led to the subspecific body‐size difference. We found that males of both subspecies preferred larger females of N. v. viridescens as mates presumably because of the fecundity advantage of larger females. On the other hand, no evidence of female choice was found. Larger males of N. v. viridescens exhibited greater competitive ability and gained primary access to larger females of their own kind. However, smaller males were able to overcome their inferior competitive ability by interfering with larger males' spermatophore transfer and sneakily mating with larger females. Thus, the subspecific body‐size difference importantly affected sexual selection processes, resulting in nonrandom but not completely assortative mating patterns between the larger and smaller subspecies. Although life‐cycle polyphenism facilitates the intraspecific ecological divergence within N. v. viridescens sexual selection processes, namely smaller males' mate preference for larger females and sexual interference during spermatophore transfer, may be halting completion of the ecological speciation. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 884–897.     

Habitat primary production and the evolution of body size within the hartebeest clade

Local adaptation is a key process in the evolution of biological diversity but relatively few studies have identified the selective forces that drive trait divergence at low taxonomic levels, particularly amongst mammals. Variation in body size across taxa is fundamental as shown by allometric relationships with numerous physiological, morphological and life-history traits. Differences in adult size across cohorts within populations of temperate ungulates are determined by variation in trophic resource availability during growth, suggesting that natural selection might promote the evolution of size divergence across sister taxa through local adaptation to variation in habitat productivity. We tested this hypothesis in the hartebeest ( Alcelaphu s sp.), an antelope lineage including eight extant (or recently extinct) allopatric subspecies that evolved within the last million years and colonized all the African savannahs. We predicted that body size across the subspecies should correlate positively with habitat productivity across taxon ranges. Mean body size of all the hartebeest taxa was quantified using skull length from museum specimens, and climatic variables were used as surrogates of habitat productivity. Body size across subspecies was positively correlated with rainfall, suggesting that variation in habitat primary production may drive morphological evolution between taxa. Focusing at a low taxonomic level has allowed us to identify a critical selective force that may shape divergence in body size, without the confounding effect of variation in trophic niche. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 431–440.     

Is size‐assortative mating important for rapid pigment differentiation in a freshwater isopod?

Identifying mechanisms behind assortative mating is central to the understanding of ecological divergence and speciation. Recent studies show that populations of the freshwater isopod Asellus aquaticus can rapidly become locally differentiated when submerged Chara vegetation expands in lakes. In the novel Chara habitat, isopods have become lighter pigmented and smaller than in ancestral reed stands. In this study, we used a laboratory multiple-choice experiment to investigate assortative mating as a possible prezygotic reproductive barrier between Chara and reed isopods. Mating was assortative when Chara isopods were experimentally mixed with isopods from an adjacent reed site with large-size individuals, suggesting a partial prezygotic reproductive barrier. No deviation from random mating could, however, be detected when Chara isopods were mixed with smaller sized isopods from another reed site. In both experiments, assortative mating was apparently based on size, as Chara isopods were larger and reed isopods smaller in mixed pairs than in assortative pairs. Pigmentation did not have any clear influence on mating. We suggest that divergence in pigmentation evolved through natural selection in conjunction with size-assortative mating indirectly causing assortative mating between Chara and reed isopods. Size-assortative mating is likely a by-product of natural selection, but its importance may hypothetically be transient, if selection erodes the correlation between pigmentation and size over time.