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.     

Mechanisms of rapid sympatric speciation by sex reversal and sexual selection in cichlid fish

Mechanisms of speciation in cichlid fish were investigated by analyzing population genetic models of sexual selection on sex-determining genes associated with color polymorphisms. The models are based on a combination of laboratory experiments and field observations on the ecology, male and female mating behavior, and inheritance of sex-determination and color polymorphisms. The models explain why sex-reversal genes that change males into females tend to be X-linked and associated with novel colors, using the hypothesis of restricted recombination on the sex chromosomes, as suggested by previous theory on the evolution of recombination. The models reveal multiple pathways for rapid sympatric speciation through the origin of novel color morphs with strong assortative mating that incorporate both sex-reversal and suppressor genes. Despite the lack of geographic isolation or ecological differentiation, the new species coexists with the ancestral species either temporarily or indefinitely. These results may help to explain different patterns and rates of speciation among groups of cichlids, in particular the explosive diversification of rock-dwelling haplochromine cichlids.     

昆虫同域物种形成机制及检验

从生物学、生态和遗传的角度阐述昆虫同域物种形成过程中涉及到的可能性机制。昆虫同域种的分化与作用于同域初始种群的歧化选择密切相关,歧化选择间接导致种群生态特征和遗传特征的分化,促进同域近缘种群间的生殖隔离。同域物种形成的过程中涉及到性状替换、性选择、同型交配等机制。寄主专化型多见于昆虫同域种的分化过程中,一般以植食性昆虫为主。有关昆虫同域物种形成的检验机制有多种,归纳起来主要包括同型交配的检验、遗传漂流的量化、遗传分化程度和连锁不平衡(LD)的检测、杂交后代适合度的估算等。目前发现在许多昆虫种类中存在同域物种形成的可能性,但是有关其隔离机制并没有得到充分的解释。     

INCIPIENT REPRODUCTIVE ISOLATION BETWEEN TWO SYMPATRIC MORPHS OF THE INTERTIDAL SNAIL LITTORINA SAXATILIS

The study of speciation in recent populations is essentially a study of the evolution of reproductive isolation mechanisms between sub-groups of a species. Prezygotic isolation can be of central importance to models of speciation, either being a consequence of reinforcement of assortative mating in hybrid zones, or a pleiotropic effect of morphological or behavioral adaptation to different environments. To suggest speciation by reinforcement between incipient species one must at least know that gene flow occurs, or have recently occurred, and that assortative mating has been established in the hybrid zone. In Galician populations of the marine snail Littorina saxatilis, two main morphs appear on the same shores, one on the upper-shore barnacle belt and the other in the lower-shore mussel belt. The two morphs overlap in distribution in the midshore where hybrids are found together with pure forms. Allozyme variation indicates that the two parental morphs share a common gene pool, although within shores, gene flow between morphs is less than gene flow within morphs. In this study, we observed mating behavior in the field, and we found that mating was not random in midshore sites, with a deficiency of heterotypic pairs. Habitat selection, assortative mating, and possibly sexual selection among females contributed to the partial reproductive isolation between the pure morphs. Sizes of mates were often positively correlated, in particular, in the upper shore, indicating size-assortative mating too. However, this seemed to be a consequence of nonrandom microdistributions of snails of different sizes. Because we also argue that the hybrid zone is of primary rather than secondary origin, this seems to be an example of sympatric reproductive isolation, either established by means of reinforcement or as a by-product to divergent selection acting on other characters.     

STRONG ASSORTATIVE MATING BY DIET,COLOR, SIZE,AND MORPHOLOGY BUT LIMITED PROGRESS TOWARD SYMPATRIC SPECIATION IN A CLASSIC EXAMPLE: CAMEROON CRATER LAKE CICHLIDS

Models predict that sympatric speciation depends on restrictive parameter ranges, such as sufficiently strong disruptive selection and assortative mating, but compelling examples in nature have rarely been used to test these predictions. I measured the strength of assortative mating within a species complex of Tilapia in Lake Ejagham, Cameroon, a celebrated example of incipient sympatric adaptive radiation. This species complex is in the earliest stages of speciation: morphological and ecological divergence are incomplete, species differ primarily in breeding coloration, and introgression is common. I captured 27 mated pairs in situ and measured the diet, color, size, and morphology of each individual. I found strong assortative mating by color, size, head depth, and dietary source of benthic or pelagic prey along two independent dimensions of assortment. Thus, Ejagham Tilapia showed strong assortative mating most conducive to sympatric speciation. Nonetheless, in contrast to a morphologically bimodal Sarotherodon cichlid species pair in the lake, Ejagham Tilapia show more limited progress toward speciation, likely due to insufficient strength of disruptive selection on morphology estimated in a previous study (γ = 0.16). This supports the predicted dependence of sympatric speciation on strong assortment and strong disruptive selection by examining a potentially stalled example in nature.     

Mate choice and the genetic basis for colour variation in a polymorphic dart frog: inferences from a wild pedigree

Understanding how reproductive barriers evolve during speciation remains an important question in evolution. Divergence in mating preferences may be a common first step in this process. The striking colour pattern diversity of strawberry dart frog (Dendrobates pumilio) populations has likely been shaped by sexual selection. Previous laboratory studies have shown that females attend to male coloration and prefer to court with males of their own colour, suggesting that divergent morphs may be reproductively isolated. To test this hypothesis, we used molecular data to estimate pedigree relationships from a polymorphic population. Whereas in the laboratory both red and yellow females preferred to court with males of their own phenotype, our pedigree shows a pattern of assortative mating only for red females. In the wild, yellow females appear to be less choosy about their mates, perhaps because they incur higher costs associated with searching than females of the more common red phenotype. We also used our pedigree to investigate the genetic basis for colour-pattern variation. The phenotype frequencies we observed were consistent with those expected if dorsal background coloration is controlled by a single locus, with complete dominance of red over yellow. Our results not only help clarify the role of sexual selection in reducing gene flow, but also shed light on the mechanisms underlying colour-pattern variation among sympatric colour morphs. The difference we observed between mating preferences measured under laboratory conditions and the pattern of mate choice observed in the wild highlight the importance of field studies for understanding behavioural reproductive isolation.     

COLOR ASSORTATIVE MATING CONTRIBUTES TO SYMPATRIC DIVERGENCE OF NEOTROPICAL CICHLID FISH

It is still debated vigorously whether sexual selection can result in speciation without physical barriers to gene flow. In this study, we used field data and molecular methods to investigate the gold–normal color polymorphism in two endemic cichlid fish species of crater lake Xiloá, Nicaragua. We found significant assortative mating by color in both Amphilophus xiloaensis and A. sagittae . Focusing on A. xiloaensis , microsatellite allele frequencies, an assignment test, and model-based cluster analysis demonstrates significant and clear genetic differentiation ( F _ST= 0.03) between gold and normal individuals in sympatry. In addition, we find genetic differentiation between all three sympatric and ecologically distinct Midas cichlid species of Lake Xiloá, A. amarillo , A. sagittae , and A. xiloaensis ( F _ST= 0.03 – 0.19), and clear genetic isolation of these species from their closest relative ( A. citrinellus ) in the neighboring great lake Managua. The A. xiloaensis gold morph is genetically more distinct from the lake's other two Midas cichlid species than is A. xiloaensis -normal. Thus, we have identified sexual isolation based on color that is evident in population genetics and mate choice. Our results suggest that sexual selection through color assortative mating may play an important role in incipient sympatric speciation in Midas cichlids of Nicaragua.     

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.     

Variance in reproductive success and the opportunity for selection in a serially monogamous species: simulations of the mating system of <Emphasis Type="Italic">Tropheus</Emphasis> (Teleostei: Cichlidae)

Sexual selection is believed to play a major role in speciation processes of cichlid fishes in the East African Great Lakes, in particular Lakes Malawi and Victoria, by driving diversification in male nuptial coloration. In Lake Tanganyika, a high rate of color pattern diversification is found in the genus Tropheus, where more than 100, mostly allopatric, color morphs have been described. Whether color pattern differentiation in Tropheus could follow from sexual selection as well, has not yet been conclusively shown. Unlike typical sexually selected species, Tropheus are sexually monomorphic, establish temporary pair bonds and spawn monogamously. Variance in mating success among individuals would still allow for sexual selection, but due to their high population census sizes, parentage data from natural populations are difficult to obtain. Simulations designed according to existing data on mating behavior in Tropheus suggested that variance in male reproductive success can be substantial and lead to levels of opportunity for selection, which are similar to values estimated, for example, from natural populations of sexually dimorphic songbirds. Variance in male success was mostly affected by the way females perceived and reacted to differences between males, and to a lesser extent by the duration of components of the reproductive cycles of males and females. These results indicate that future work on the importance of sexual selection in Tropheus should concentrate on mate choice cues and female mate choice behavior, but does not depend critically on the acquisition of more detailed life history data.     

Male mating preferences pre-date the origin of a female trait polymorphism in an incipient species complex of Lake Victoria cichlids

Disruptive sexual selection on colour patterns has been suggested as a major cause of diversification in the cichlid species flock of Lake Victoria. In Neochromis omnicaeruleus, a colour and sex determination polymorphism is associated with a polymorphism in male and female mating preferences. Theoretical work on this incipient species complex found conditions for rapid sympatric speciation by selection on sex determination and sexual selection on male and female colour patterns, under restrictive assumptions. Here we test the biological plausibility of a key assumption of such models, namely, the existence of a male preference against a novel female colour morph before its appearance in the population. We show that most males in a population that lacks the colour polymorphism exhibit a strong mating preference against the novel female colour morph and that reinforcement is not a likely explanation for the origin of such male preferences. Our results show that a specific condition required for the combined action of selection on sex determination and sexual selection to drive sympatric speciation is biologically justified. Finally, we suggest that Lake Victoria cichlids might share an ancestral female recognition scheme, predisposing colour monomorphic populations/species to similar evolutionary pathways leading to divergence of colour morphs in sympatry.     

Extraordinary AFLP fingerprint similarity despite strong assortative mating between reef fish color morphospecies

Recent theoretical models and empirical studies of fruit flies, birds, and fish indicate that assortative mating may initiate speciation when physical barriers to gene flow are absent, and before postzygotic barriers evolve. These are important results for marine animals like coral reef fish, where ocean currents can carry planktonic larvae over broad ranges, interconnecting populations and slowing genetic divergence. The Caribbean hamlets (genus Hypoplectrus) are a flock of reef fish morphospecies with highly distinct color pattern that mate like with like, but show little mitochondrial or microsatellite DNA differentiation. Here, we broadly screen genomic diversity using amplified fragment length polymorphisms (AFLP) and survey mating pair formation between two morphospecies in the Florida Keys, the butter hamlet (H. unicolor) and the blue hamlet (H. gemma). No AFLP was species-diagnostic (fixed), and neighbor-joining analyses revealed no clustering of individuals consistent with morphospecies boundaries. Assignment tests, however, placed most individuals within their morphospecies of origin. Field surveys showed that > 98% of mating pairs, including those of rare morphospecies, were of like color pattern. Spawning by a single mixed pair adds to earlier observations suggesting that infrequent hybridization may be a genetically homogenizing force in Hypoplectrus. This study provides a clear example of strong assortative mating in a system with limited genetic differentiation.     

Color polymorphism and sex ratio distortion in a cichlid fish as an incipient stage in sympatric speciation by sexual selection

We investigated a Lake Victoria cichlid with a complex colour polymorphism that apparently represents one original species and two incipient species, all of which are sympatric. In laboratory breeding experiments we observed sex ratio distortion in certain matings between original and incipient species. Mate choice experiments show that males of the incipient species exhibit mating preferences against the original species, and males and females of the original species exhibit strong mating preferences against the incipient species. Mating preferences might evolve by sex ratio selection to avoid matings with distorted progeny sex ratios. Phenotype frequencies in nature suggest that mating preferences translate into mating frequencies, thus restricting gene flow and exerting disruptive sexual selection between the original and incipient species. The incipient species do not differ in morphology or ecology from the original species, implying that colour polymorphism, associated with sex ratio distortion, can be an incipient stage in sympatric speciation, and that disruption of gene flow can precede ecological differentiation.     

Multiple speciation events in an arthropod with divergent evolution in sexual morphology

Sexual selection can facilitate divergent evolution of traits related to mating and consequently promote speciation. Theoretically, independent operation of sexual selection in different populations can lead to divergence of sexual traits among populations and result in allopatric speciation. Here, we show that divergent evolution in sexual morphology affecting mating compatibility (body size and genital morphologies) and speciation have occurred in a lineage of millipedes, the Parafontaria tonominea species complex. In this millipede group, male and female body and genital sizes exhibit marked, correlated divergence among populations, and the diverged morphologies result in mechanical reproductive isolation between sympatric species. The morphological divergence occurred among populations independently and without any correlation with climatic variables, although matching between sexes has been maintained, suggesting that morphological divergence was not a by-product of climatic adaptation. The diverged populations underwent restricted dispersal and secondary contact without hybridization. The extent of morphological difference between sympatric species is variable, as is diversity among allopatric populations; consequently, the species complex appears to contain many species. This millipede case suggests that sexual selection does contribute to species richness via morphological diversification when a lineage of organisms consists of highly divided populations owing to limited dispersal.     

POSTZYGOTIC GENETIC INCOMPATIBILITY BETWEEN SYMPATRIC COLOR MORPHS

Alternative genetically determined color morphs within a population or species are believed to successfully interbreed within a population. However, the occurrence of prezygotic or ecological selection in a number of polymorphic systems may lead to nonrandom mating and prevent genetic morphs from fully interbreeding. Here we show that postzygotic incompatibility significantly limits gene flow between the sympatric red and black color morphs of the Gouldian finch ( Erythrura gouldiae ). Using a balanced within-female experimental design, in which individuals were forced to breed in pure and mixed morph crosses, we found large inviability effects (>30%) in offspring resulting from genetically mixed genotypes. The consistent mortality effects across different stages of development (e.g., prehatching, juvenile, adulthood), unconfounded by environmentally derived parental effects or social environments, reveal an underlying genetic incompatibility between different genotypes. Furthermore, mortality in mixed morph genotypes was particularly severe (43.6%) for the heterogametic sex (daughters), which is consistent with Haldane's rule predicted for postzygotic incompatibilities between hybridizing species. This significant, but incomplete, postzygotic isolation suggests that the sympatric morphs may represent transient stages in the speciation–hybridization process.     

Parallel evolution of sexual isolation in sticklebacks

Mechanisms of speciation are not well understood, despite decades of study. Recent work has focused on how natural and sexual selection cause sexual isolation. Here, we investigate the roles of divergent natural and sexual selection in the evolution of sexual isolation between sympatric species of threespine sticklebacks. We test the importance of morphological and behavioral traits in conferring sexual isolation and examine to what extent these traits have diverged in parallel between multiple, independently evolved species pairs. We use the patterns of evolution in ecological and mating traits to infer the likely nature of selection on sexual isolation. Strong parallel evolution implicates ecologically based divergent natural and/or sexual selection, whereas arbitrary directionality implicates nonecological sexual selection or drift. In multiple pairs we find that sexual isolation arises in the same way: assortative mating on body size and asymmetric isolation due to male nuptial color. Body size and color have diverged in a strongly parallel manner, similar to ecological traits. The data implicate ecologically based divergent natural and sexual selection as engines of speciation in this group.     

Molecular phylogeny of the Puerto Rican Lepidocyrtus and Pseudosinella (Hexapoda: Collembola), a validation of Yoshii's "color pattern species"

Color pattern was one of the most important characters used to diagnose species in the genus Lepidocyrtus until the introduction of chaetotaxy to Collembola taxonomy. Chaetotaxy confirmed most species diagnoses based only on color patterns, but a number of populations with distinct pigmentation patterns have been found to be identical in all other morphological characters. The absence of individuals showing intermediate color patterns prompted Yoshii to suggest that, despite chaetotaxic identity, populations with distinct color forms represent valid species (implying reproductive isolation and therefore biological species) in what he designated as "color pattern species." In Puerto Rico Lepidocyrtus biphasis, L. dispar, and L. caprilesi show a remarkable variation in pigmentation and as a group include 11 different color forms. Here I present a phylogenetic analysis of the cytochrome oxidase I gene (COI) in 17 species of Lepidocyrtus and Pseudosinella, including 11 species and 10 color forms of Puerto Rican Lepidocyrtus, to test Yoshii's color pattern species concept. The analysis shows large genetic distances between species defined based on morphology alone (morphospecies) and between most color variants within morphospecies. The most often used calibration for the COI molecular clock (2.3% sequence divergence per million years) suggests that morphospecies diverged between 20 and 25 million years before present while color forms within morphospecies diverged between 8 and 19 million years ago. This indicates that changes in climate and sea levels during the Pleistocene were irrelevant to the speciation process in the Puerto Rican Lepidocyrtus. Examination of the genetic variation, phylogenetic relationships, and collection data in light of the biological and phylogenetic species concepts supports the hypothesis that most populations of morphospecies differing only in color pattern are distinct species, thus validating Yoshii's color pattern species concept. As a result it is suggested that morphological characters traditionally used in species diagnoses are very conservative indicators of genetic divergence, that the diversity of springtails has been greatly underestimated, and that studies concerned with identifying factors promoting speciation in Collembola could be misled if they do not include analysis of mitochondrial markers.     

Regional divergence and mosaic spatial distribution of two closely related damselfly species (Enallagma hageni and Enallagma ebrium)

North American Enallagma damselflies radiated during the Pleistocene, and species differ mainly by reproductive structures. Although morphologically very different, Enallagma hageni and Enallagma ebrium are genetically very similar. Partitioning of genetic variation (AFLP), isolation by distance and clustering analyses indicate that these morphospecies are locally differentiated genetically. Spatial analyses show that they are rarely sympatric at local sites, and their distributions form a mosaic of patches where one is clearly dominant over hundreds of square kilometers. However, these morphospecies are also not genetically more similar when they are sympatric, indicating that hybridization is probably not occurring. Given that these morphospecies are ecologically equivalent, strong assortative mating, reproductive interference and fast post-glacial recolonization may explain the origin and maintenance of these distributional patches across eastern North America. By limiting opportunities for gene flow, reproductive interference may play an unsuspected role in accelerating genetic differentiation in the early phases of nonecological speciation.     

Competitive environments induce shifts in host fidelity

Recent models support the idea of sympatric speciation as a result of the joint effects of disruptive selection and assortative mating. We present experimental data, testing models of speciation through frequency‐dependent selection. We show that under high competition on a mixture of resources/hosts, strains of the Seed beetle, Callosobruchus maculatus, change their host fidelity and evolve a more generalistic behaviour in resource utilization among females. The change in host fidelity did not result in disruptive selection and was not followed by assortative mating. This means that only one of three fundamental prerequisites for sympatric speciation evolved as a result of the frequency‐dependent selection. We conclude that for this process to work, a shift to a novel food resource as a result of selection must also lead to a loss of preference for the original resource such that individuals are only able to use either one of the two.     

Polymorphism and speciation in Arctic charr

The Arctic charr Salvelinus alpinus exhibits 1–4 sympatric morphs in postglacial lakes, of which one or two are epibenthic zoobenthos feeders, one is a limnetic planktivore and one is a piscivorous form. In addition, northern rivers support partly migratory populations with anadromous and freshwater resident fish. The morphs vary in their coloration, morphology, life history, behaviour and genetic characteristics. The morphs usually differentiate according to their ontogenetic stage at maturity, which parallels paedomorphism in amphibians. The young usually start as epibenthic zoobenthivores, but may become pelagic at a certain size according to the predation risk experienced at that time. From a length of > 20–25 cm, charr start to become piscivorous. The proportion of piscivorous fish increases with increasing body size. In partly anadromous populations, fish that mature before smolting become freshwater resident, the others anadromous. In some rivers, the morphs occupy separate niches (epibenthic and limnetic), from emergence onwards. The morphs exhibit different degrees of reproductive isolation that vary from a high degree of interbreeding to complete isolation. Usually, they spawn within morph (assortative mating), but alternative male mating behaviour (sneaking, fighting) may occur in stream‐spawning populations and at great depths in lakes. Morphologically specialized morphs appear to feed more effectively than intermediate forms, and selection according to feeding mode, site fidelity and associated assortative mating are prerequisites for the evolution of the different morphs. Charr morphs develop into stable feeding niches under conditions of intense intraspecific competition when there is little competition with other species. Sympatric morphs exhibit different degrees of speciation, but similar morphs in different systems are not individual species because of (1) their polyphyletic origin, (2) the supporting systems are often young, transient environments making the future situation for the populations uncertain, and (3) the genetic differentiation among morphs is low. Sympatric morphs may interbreed and produce fertile hybrids. Nevertheless, sympatric charr morphs should be managed as separate species. Changes in the natural conditions or human impacts to which the morphs are adapted will have a strong influence on the persistence and survival of each different morph.