A quantitative genetic competition model for sympatric speciation

I use multilocus genetics to describe assortative mating in a competition model. The intensity of competition between individuals is influenced by a quantitative character whose value is determined additively by alleles from many loci. With assortative mating based on this character, frequency- and density-dependent competition can subdivide a population with an initially unimodal character distribution. The character distribution becomes bimodal, and the subpopulations corresponding to the two modes are reproductively separated because mating is assortative. This happens if the resource distribution is unimodal, i.e. even if selection due to phenotypic carrying capacities is not disruptive. The results suggest that sympatric speciation due to frequency-dependent selection can occur in quite general ecological scenarios if mating is assortative. I also discuss the evolution of assortative mating. Since it induces bimodal phenotype distributions, assortative mating leads to a better match of the resources if their distribution is also bimodal. Moreover, in a population with a bimodal phenotype distribution, the average strength of frequency-dependent competition is lower than in a unimodal population. Therefore, assortative mating permits higher equilibrium densities than random mating even if the resource distribution is unimodal. Thus, even though it may lead to a less efficient resource use, assortative mating is favoured over random mating because it reduces frequency-dependent effects of competition.     

Multimodal pattern formation in phenotype distributions of sexual populations

During bouts of evolutionary diversification, such as adaptive radiations, the emerging species cluster around different locations in phenotype space. How such multimodal patterns in phenotype space can emerge from a single ancestral species is a fundamental question in biology. Frequency-dependent competition is one potential mechanism for such pattern formation, as has previously been shown in models based on the theory of adaptive dynamics. Here, we demonstrate that also in models similar to those used in quantitative genetics, phenotype distributions can split into multiple modes under the force of frequency-dependent competition. In sexual populations, this requires assortative mating, and we show that the multimodal splitting of initially unimodal distributions occurs over a range of assortment parameters. In addition, assortative mating can be favoured evolutionarily even if it incurs costs, because it provides a means of alleviating the effects of frequency dependence. Our results reveal that models at both ends of the spectrum between essentially monomorphic (adaptive dynamics) and fully polymorphic (quantitative genetics) yield similar results. This underscores that frequency-dependent selection is a strong agent of pattern formation in phenotype distributions, potentially resulting in adaptive speciation.     

Ecological speciation in postglacial European whitefish: rapid adaptive radiations into the littoral,pelagic, and profundal lake habitats

Understanding how a monophyletic lineage of a species diverges into several adaptive forms has received increased attention in recent years, but the underlying mechanisms in this process are still under debate. Postglacial fishes are excellent model organisms for exploring this process, especially the initial stages of ecological speciation, as postglacial lakes represent replicated discrete environments with variation in available niches. Here, we combine data of niche utilization, trophic morphology, and 17 microsatellite loci to investigate the diversification process of three sympatric European whitefish morphs from three northern Fennoscandian lakes. The morphological divergence in the gill raker number among the whitefish morphs was related to the utilization of different trophic niches and was associated with reproductive isolation within and across lakes. The intralacustrine comparison of whitefish morphs showed that these systems represent two levels of adaptive divergence: (1) a consistent littoral–pelagic resource axis; and (2) a more variable littoral–profundal resource axis. The results also indicate that the profundal whitefish morph has diverged repeatedly from the ancestral littoral whitefish morph in sympatry in two different watercourses. In contrast, all the analyses performed revealed clustering of the pelagic whitefish morphs across lakes suggesting parallel postglacial immigration with the littoral whitefish morph into each lake. Finally, the analyses strongly suggested that the trophic adaptive trait, number of gill rakers, was under diversifying selection in the different whitefish morphs. Together, the results support a complex evolutionary scenario where ecological speciation acts, but where both allopatric (colonization history) and sympatric (within watercourse divergence) processes are involved.     

Assortative mating by diet in a phenotypically unimodal but ecologically variable population of stickleback

Speciation with gene flow may be driven by a combination of positive assortative mating and disruptive selection, particularly if selection and assortative mating act on the same trait, eliminating recombination between ecotype and mating type. Phenotypically unimodal populations of threespine stickleback (Gasterosteus aculeatus) are commonly subject to disruptive selection due to competition for alternate prey. Here we present evidence that stickleback also exhibit assortative mating by diet. Among-individual diet variation leads to variation in stable isotopes, which reflect prey use. We find a significant correlation between the isotopes of males and eggs within their nests. Because egg isotopes are derived from females, this correlation reflects assortative mating between males and females by diet. In concert with disruptive selection, this assortative mating should facilitate divergence. However, the stickleback population remains phenotypically unimodal, highlighting the fact that assortative mating and disruptive selection do not guarantee evolutionary divergence and speciation.     

Disruptive natural selection predicts divergence between the sexes during adaptive radiation

Evolution of sexual dimorphism in ecologically relevant traits, for example, via resource competition between the sexes, is traditionally envisioned to stall the progress of adaptive radiation. An alternative view is that evolution of ecological sexual dimorphism could in fact play an important positive role by facilitating sex‐specific adaptation. How competition‐driven disruptive selection, ecological sexual dimorphism, and speciation interact during real adaptive radiations is thus a critical and open empirical question. Here, we examine the relationships between these three processes in a clade of salamanders that has recently radiated into divergent niches associated with an aquatic life cycle. We find that morphological divergence between the sexes has occurred in a combination of head shape traits that are under disruptive natural selection within breeding ponds, while divergence among species means has occurred independently of this disruptive selection. Further, we find that adaptation to aquatic life is associated with increased sexual dimorphism across taxa, consistent with the hypothesis of clade‐wide character displacement between the sexes. Our results suggest the evolution of ecological sexual dimorphism may play a key role in niche divergence among nascent species and demonstrate that ecological sexual dimorphism and ecological speciation can and do evolve concurrently in the early stages of adaptive radiation.     

Correlational selection and the evolution of genomic architecture

We review and discuss the importance of correlational selection (selection for optimal character combinations) in natural populations. If two or more traits subject to multivariate selection are heritable, correlational selection builds favourable genetic correlations through the formation of linkage disequilibrium at underlying loci governing the traits. However, linkage disequilibria built up by correlational selection are expected to decay rapidly (ie, within a few generations), unless correlational selection is strong and chronic. We argue that frequency-dependent biotic interactions that have 'Red Queen dynamics' (eg, host-parasite interactions, predator-prey relationships or intraspecific arms races) often fuel chronic correlational selection, which is strong enough to maintain adaptive genetic correlations of the kind we describe. We illustrate these processes and phenomena using empirical examples from various plant and animal systems, including our own recent work on the evolutionary dynamics of a heritable throat colour polymorphism in the side-blotched lizard Uta stansburiana. In particular, male and female colour morphs of side-blotched lizards cycle on five- and two-generation (year) timescales under the force of strong frequency-dependent selection. Each morph refines the other morph in a Red Queen dynamic. Strong correlational selection gradients among life history, immunological and morphological traits shape the genetic correlations of the side-blotched lizard polymorphism. We discuss the broader evolutionary consequences of the buildup of co-adapted trait complexes within species, such as the implications for speciation processes.     

Colour pattern as a single trait driving speciation in Hypoplectrus coral reef fishes?

Theory shows that speciation in the presence of gene flow occurs only under narrow conditions. One of the most favourable scenarios for speciation with gene flow is established when a single trait is both under disruptive natural selection and used to cue assortative mating. Here, we demonstrate the potential for a single trait, colour pattern, to drive incipient speciation in the genus Hypoplectrus (Serranidae), coral reef fishes known for their striking colour polymorphism. We provide data demonstrating that sympatric Hypoplectrus colour morphs mate assortatively and are genetically distinct. Furthermore, we identify ecological conditions conducive to disruptive selection on colour pattern by presenting behavioural evidence of aggressive mimicry, whereby predatory Hypoplectrus colour morphs mimic the colour patterns of non-predatory reef fish species to increase their success approaching and attacking prey. We propose that colour-based assortative mating, combined with disruptive selection on colour pattern, is driving speciation in Hypoplectrus coral reef fishes.     

Recent speciation and secondary contact in endemic ants

Gene flow is the main force opposing divergent selection, and its effects are greater in populations in close proximity. Thus, complete reproductive isolation between parapatric populations is not expected, particularly in the absence of ecological adaptation and sharp environmental differences. Here, we explore the biogeographical patterns of an endemic ant species, Cataglyphis floricola, for which two colour morphs (black and bicolour) coexist in parapatry throughout continuous sandy habitat in southern Spain. Discriminant analyses of six biometric measurements of male genitalia and 27 cuticular hydrocarbons reveal high differentiation between morphs. Furthermore, the low number of shared alleles derived from nuclear markers (microsatellites) between the morphs at their contact zone suggests the absence of recent gene flow. Mitochondrial DNA (COI) phylogenetic analysis and median‐joining networks show that the black morph is basal to the bicolour morph, with unique haplotypes recovered for each morph. Mismatch distribution analysis and Bayesian skyline plots suggest that they are undergoing different demographic changes, with the bicolour and black morphs at demographic equilibrium and expansion, respectively. Thus, our results show complete reproductive isolation between the two colour morphs as evidenced from genetic, chemical and morphological data. We suggest that these divergence events could be explained by historical vicariance during the Pleistocene, in which reproductive traits experienced strong divergent selection between the morphs initiating or culminating speciation.     

The conditions for speciation through intraspecific competition

Abstract It has been shown theoretically that sympatric speciation can occur if intraspecific competition is strong enough to induce disruptive selection. However, the plausibility of the involved processes is under debate, and many questions on the conditions for speciation remain unresolved. For instance, is strong disruptive selection sufficient for speciation? Which roles do genetic architecture and initial composition of the population play? How strong must assortative mating be before a population can split in two? These are some of the issues we address here. We investigate a diploid multilocus model of a quantitative trait that is under frequency‐dependent selection caused by a balance of intraspecific competition and frequency‐independent stabilizing selection. This trait also acts as mating character for assortment. It has been established previously that speciation can occur only if competition is strong enough to induce disruptive selection. We find that speciation becomes more difficult for very strong competition, because then extremely strong assortment is required. Thus, speciation is most likely for intermediate strengths of competition, where it requires strong, but not extremely strong, assortment. For this range of parameters, however, it is not obvious how assortment can evolve from low to high levels, because with moderately strong assortment less genetic variation is maintained than under weak or strong assortment sometimes none at all. In addition to the strength of frequency‐dependent competition and assortative mating, the roles of the number of loci, the distribution of allelic effects, the initial conditions, costs to being choosy, the strength of stabilizing selection, and the particular choice of the fitness function are explored. A multitude of possible evolutionary outcomes is observed, including loss of all genetic variation, splitting in two to five species, as well as very short and extremely long stable limit cycles. On the methodological side, we propose quantitative measures for deciding whether a given distribution reflects two (or more) reproductively isolated clusters.     

Sexual dimorphism and adaptive speciation: two sides of the same ecological coin

Models of adaptive speciation are typically concerned with demonstrating that it is possible for ecologically driven disruptive selection to lead to the evolution of assortative mating and hence speciation. However, disruptive selection could also lead to other forms of evolutionary diversification, including ecological sexual dimorphisms. Using a model of frequency-dependent intraspecific competition, we show analytically that adaptive speciation and dimorphism require identical ecological conditions. Numerical simulations of individual-based models show that a single ecological model can produce either evolutionary outcome, depending on the genetic independence of male and female traits and the potential strength of assortative mating. Speciation is inhibited when the genetic basis of male and female ecological traits allows the sexes to diverge substantially. This is because sexual dimorphism, which can evolve quickly, can eliminate the frequency-dependent disruptive selection that would have provided the impetus for speciation. Conversely, populations with strong assortative mating based on ecological traits are less likely to evolve a sexual dimorphism because females cannot simultaneously prefer males more similar to themselves while still allowing the males to diverge. This conflict between speciation and dimorphism can be circumvented in two ways. First, we find a novel form of speciation via negative assortative mating, leading to two dimorphic daughter species. Second, if assortative mating is based on a neutral marker trait, trophic dimorphism and speciation by positive assortative mating can occur simultaneously. We conclude that while adaptive speciation and ecological sexual dimorphism may occur simultaneously, allowing for sexual dimorphism restricts the likelihood of adaptive speciation. Thus, it is important to recognize that disruptive selection due to frequency-dependent interactions can lead to more than one form of adaptive splitting.     

Sexual dimorphism and speciation on two ecological coins: patterns from nature and theoretical predictions

Adaptive divergence of phenotypes, such as sexual dimorphism or adaptive speciation, can result from disruptive selection via competition for limited resources. Theory indicates that speciation and sexual dimorphism can result from identical ecological conditions, but co-occurrence is unlikely because whichever evolves first should dissipate the disruptive selection necessary to drive evolution of the other. Here, we consider ecological conditions in which disruptive selection can act along multiple ecological axes. Speciation in lake populations of threespine sticklebacks (Gasterosteus aculeatus) has been attributed to disruptive selection due to competition for resources. Head shape in sticklebacks is thought to reflect adaptation to different resource acquisition strategies. We measure sexual dimorphism and species variation in head shape and body size in stickleback populations in two lakes in British Columbia, Canada. We find that sexual dimorphism in head shape is greater than interspecific differences. Using a numerical simulation model that contains two axes of ecological variation, we show that speciation and sexual dimorphism can readily co-occur when the effects of loci underlying sexually dimorphic traits are orthogonal to those underlying sexually selected traits.     

Evolutionary dynamics through multispecies competition

Disruptive selection, emerging from frequency-dependent intraspecific competition can have very exciting evolutionary outcomes. One such outcome is the origin of new species through an evolutionary branching event. Literature on theoretical models investigating the emergence of disruptive selection is vast, with some investigating the sensitivity of the models on assumptions of the competition and carrying capacity functions’ shapes. What is seldom modeled is what happens once the population escapes its effect via increase phenotypic or genotypic variance. The expectation is mixed: disruptive selection could diminish and ultimately disappear or it could still exist leading to further speciation events through multiple evolutionary branching events. Here, we derive the conditions under which disruptive selection drives two subpopulations that originated at a branching point to other points in trait space where each subpopulation again experiences disruptive selection. We show that the general pattern for further branchings require that the competition function to be even narrower than what is required for the first evolutionary branching. However, we also show that the existence of disruptive selection in higher dimensional systems is also sensitive to the shapes of the functions used.     

Determinants of the strength of disruptive and/or divergent selection arising from resource competition

We investigate how the intensity of competition for resources affects the strength of disruptive selection on a resource acquisition trait. This is done by analyzing several consumer–resource models in which consumers use a linear array of resources. We show that disruptive selection can be diminished under both strong and weak competition, making disruptive selection a unimodal function of the strength of competition. Weak selection under strong competition arises when competition causes the extinction (for self-reproducing resources) or depletion (for abiotic resources) of the most rapidly caught resources. Weak selection under weak competition is a consequence of minimal effects of consumers on resources. The precise relationship between intensity of competition and strength of disruptive selection is sensitive to the shape of the consumer's resource utilization curve and the nature of resource growth. The most strongly unimodal competition–selection relationships result from utilization curves with long tails. Our results show that a simple comparison of the width of the resource abundance distribution and the consumer's utilization function is not sufficient to determine whether selection is disruptive. The results may explain some contradictory experimental findings regarding the effect of consumer mortality on the strength of disruptive selection.     

Alternative trait combinations and secondary resource partitioning in sexually selected color polymorphism

Resource partitioning within a species, trophic polymorphism is hypothesized to evolve by disruptive selection when intraspecific competition for certain resources is severe. However, in this study, we reported the secondary partitioning of oviposition resources without resource competition in the damselfly Ischnura senegalensis. In this species, females show color polymorphism that has been evolved as counteradaptation against sexual conflict. One of the female morphs is a blue‐green (andromorph, male‐like morph), whereas the other morph is brown (gynomorph). These female morphs showed alternative preferences for oviposition resources (plant tissues); andromorphs used fresh (greenish) plant tissues, whereas gynomorphs used decaying (brownish) plants tissues, suggesting that they chose oviposition resources on which they are more cryptic. In addition, the two‐color morphs had different egg morphologies. Andromorphs have smaller and more elongated eggs, which seemed to adapt to hard substrates compared with those of gynomorphs. The resource partitioning in this species is achieved by morphological and behavioral differences between the color morphs that allow them to effectively exploit different resources. Resource partitioning in this system may be a by‐product of phenotypic integration with body color that has been sexually selected, suggesting an overlooked mechanism of the evolution of resource partitioning. Finally, we discuss the evolutionary and ecological consequences of such resource partitioning.     

Evidence for divergent natural selection of a Lake Tanganyika cichlid inferred from repeated radiations in body size

Divergent natural selection is thought to play a vital role in speciation, but clear, measurable examples from nature are still few. Among the many possible sources of divergent natural selection, predation pressure may be important because predators are ubiquitous in food webs. Here, we show evidence for divergent natural selection in a Lake Tanganyika cichlid, Telmatochromis temporalis , which uses burrows under stones or empty snail shells as shelters. This species contains normal and dwarf morphs at several localities. The normal morph inhabits rocky shorelines, whereas the dwarf morph invariably inhabits shell beds, where empty snail shells densely cover the lake bottom. Genetic evidence suggested that the dwarf morph evolved independently from the normal morph at two areas, and morphological analysis and evaluation of habitat structure revealed that the body sizes of morphs closely matched the available shelter sizes in their habitats. These findings suggest that the two morphs repeatedly evolved through divergent natural selection associated with the strategy for sheltering from predators.     

Intensity of male‐male competition predicts morph diversity in a color polymorphic lizard

Sexual selection is one of the main processes involved in the emergence and maintenance of heritable color polymorphisms in a variety of taxa. Here, we test whether the intensity of sexual selection, estimated from population sex ratio, predicts morph diversity in Podarcis muralis, a color polymorphic lizard with discrete white, yellow, orange, white‐orange, and yellow‐orange male and female phenotypes (i.e., morphs). In a sample of 116 Pyrenean populations and 5421 lizards, sex ratios (m/f) vary from 0.29 to 2.5, with the number of morphs for each sex ranging from 2 to 5. Male‐biased sex ratios are associated with increased morph diversity as measured with Shannon's diversity index. The main factor accounting for this relationship is male morph richness (i.e., the number of morphs). In contrast, female morph diversity is not related to sex ratio. These results suggest a relationship between the intensity of male intrasexual competition and male morph diversity. While other selective forces may interact with sexual selection in maintaining the color polymorphisms in P. muralis, this evidence suggests a complex evolutionary scenario possibly involving frequency‐dependent selection of alternative reproductive tactics and/or complex balancing selection.     

Rugged adaptive landscapes shape a complex,sympatric radiation

Strong disruptive ecological selection can initiate speciation, even in the absence of physical isolation of diverging populations. Species evolving under disruptive ecological selection are expected to be ecologically distinct but, at least initially, genetically weakly differentiated. Strong selection and the associated fitness advantages of narrowly adapted individuals, coupled with assortative mating, are predicted to overcome the homogenizing effects of gene flow. Theoretical plausibility is, however, contrasted by limited evidence for the existence of rugged adaptive landscapes in nature. We found evidence for multiple, disruptive ecological selection regimes that have promoted divergence in the sympatric, incipient radiation of ‘sharpfin’ sailfin silverside fishes in ancient Lake Matano (Sulawesi, Indonesia). Various modes of ecological specialization have led to adaptive morphological differences between the species, and differently adapted morphs display significant but incomplete reproductive isolation. Individual fitness and variation in morphological key characters show that disruptive selection shapes a rugged adaptive landscape in this small but complex incipient lake fish radiation.     

Sexual selection on phenotypic traits in a hybrid zone of Littorina saxatilis (Olivi)

Step clinal transitions in inherited character(s) between genetically distinct populations are usually referred to as hybrid zones. An example is found in the population of the intertidal snail Littorina saxatilis in Galicia (NW Spain). We studied the shape of the overall fitness surface for sexual selection in this hybrid zone, and the position of hybrids and pure morphs on this surface. We found that sexual divergent selection acted on a combination of phenotypic traits separating the pure morphs, and therefore that sexual selection contributed to morph differentiation. The average fitness of hybrids as a group was not significantly different from that of the pure morphs, but they did show divergent sexual selection in some traits. These results are in agreement with a model of divergent selection favouring both the pure morph as well as those hybrids most resembling each morph. The finding of divergent selection is remarkable because quadratic selection gradients are usually weak in nature.     

Differential foraging success across a light level spectrum explains the maintenance and spatial structure of colour morphs in a polymorphic bird

Detectability of different colour morphs under varying light conditions has been proposed as an important driver in the maintenance of colour polymorphism via disruptive selection. To date, no studies have tested whether different morphs have selective advantages under differing light conditions. We tested this hypothesis in the black sparrowhawk, a polymorphic raptor exhibiting a discrete white and dark morph, and found that prey provisioning rates differ between the morphs depending on light condition. Dark morphs delivered more prey in lower light conditions, while white morphs provided more prey in brighter conditions. We found support for the role of breeding season light level in explaining the clinal pattern of variation in morph ratio across the species range throughout South Africa. Our results provide the first empirical evidence supporting the hypothesis that polymorphism in a species, and the spatial structuring of morphs across its distribution, may be driven by differential selective advantage via improved crypsis, under varying light conditions.     

Pollinator Competition as a Driver of Floral Divergence: An Experimental Test

Optimal foraging models of floral divergence predict that competition between two different types of pollinators will result in partitioning, increased assortative mating, and divergence of two floral phenotypes. We tested these predictions in a tropical plant-pollinator system using sexes of purple-throated carib hummingbirds (Anthracothorax jugularis) as the pollinators, red and yellow inflorescence morphs of Heliconia caribaea as the plants, and fluorescent dyes as pollen analogs in an enclosed outdoor garden. When foraging alone, males exhibited a significant preference for the yellow morph of H. caribaea, whereas females exhibited no preference. In competition, males maintained their preference for the yellow morph and through aggression caused females to over-visit the red morph, resulting in resource partitioning. Competition significantly increased within-morph dye transfer (assortative mating) relative to non-competitive environments. Competition and partitioning of color morphs by sexes of purple-throated caribs also resulted in selection for floral divergence as measured by dye deposition on stigmas. Red and yellow morphs did not differ significantly in dye deposition in the competition trials, but differences in dye deposition and preferences for morphs when sexes of purple-throated caribs foraged alone implied fixation of one or the other color morph in the absence of competition. Competition also resulted in selection for divergence in corolla length, with the red morph experiencing directional selection for longer corollas and the yellow morph experiencing stabilizing selection on corolla length. Our results thus support predictions of foraging models of floral divergence and indicate that pollinator competition is a viable mechanism for divergence in floral traits of plants.