The Midas cichlid species complex: incipient sympatric speciation in Nicaraguan cichlid fishes?

Abstract Sympatric speciation is a contentious concept, although theoretical models as well as empirical evidence support its relevance in evolutionary biology. The Midas cichlid species complex (Amphilophus citrinellus, labiatus, zaliosus) from several crater lakes in Nicaragua fits several of the key characteristics of a sympatric speciation model. In particular, in A. citrinellus (i) strong assortative mating on the basis of colour polymorphism and (ii) ecological differentiation based on morphological polymorphisms involving the feeding apparatus and body shape might both be mechanisms of incipient speciation. Seven microsatellite markers and mtDNA control region sequences [836 base pairs (bp)] were used to study the population genetic structure of 519 specimens of Midas cichlid populations from the two Great Lakes Managua and Nicaragua, and three crater lakes in Nicaragua, Central America. The three named species of the species complex occupy different ecological niches, are morphologically distinct and can be distinguished genetically. We uncovered allopatric genetic differentiation of populations of A. citrinellus from different lakes and distant locations within Lake Managua and, more interestingly, incipient genetic differentiation of several sympatric populations based on colouration (in A. citrinellus and A. labiatus) but not on the morphology of the pharyngeal jaws (in A. citrinellus). Sexual selection and assortative mating might be the driven forces of diversification within named species. The Midas cichlid species complex in Nicaragua is an excellent model system for the study of the incipient stages of adaptation, speciation and the formation of species flocks.     

Trophic polymorphism in a riverine fish: morphological, dietary, and genetic analysis of mountain whitefish

Trophic polymorphisms are a prominent form of phenotypic diversification in many animal taxa. Northern temperate lakes have become model systems for the investigation of sympatric speciation due to trophic polymorphisms. Many examples of niche-based phenotypic variation occur in temperate lakes, whereas northern rivers offer few such examples. To further investigate the conditions under which trophic polymorphisms are likely to evolve, the present study examined phenotypic variation related to snout size and shape in the mountain whitefish (Salmonidae: Prosopium williamsoni ), which has been hypothesized to exhibit a rare example of reproductively isolated trophic morphs in a northern river-dwelling fish species. Variation in snout size and shape increased greatly with body size and, although this variation was continuously distributed, individuals in the largest size class tended to lie at phenotypic extremes. At one extreme were individuals with a large bulbous snout and a sloping forehead ('pinocchio'), and at the other were individuals that lack the bulbous snout and have a concave forehead ('normal'). The pinocchio trait may result from a stage-specific developmental switch that occurs late in ontogeny. Consistent differences were found with respect to diet between individuals with extreme snout morphologies, but no evidence was found for assortative mating within populations at seven microsatellite loci. The explosive mating system of this species may be responsible for this lack of assortative mating. The present study highlights the influence of ecological factors in shaping phenotypic and behavioural diversification due to trophic morphology.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 253–267.     

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.     

Labile ecotypes accompany rapid cladogenesis in an adaptive radiation of Mandarina (Bradybaenidae) land snails

The endemic land snail genus Mandarina of the oceanic Bonin Islands shows exceptionally diverse morphological and ecological traits. Previous studies have already provided evidence that speciation on different islands of the three main archipelagos was such that similar ecotypes evolved independently in different lineages and islands. Here we present data to show that the same species can have different ecotypes. As most of the characters involved are inherited, then variation between ecotypes must represent genetic differences between populations. We then show that the radiation on the Bonin Islands is derived from a single colonization event, and use a mitochondrial phylogeny to provide evidence for a burst of cladogenesis soon after colonization. As divergent selection has previously been implicated in causing differences between Mandarina species, and theory predicts that most of the speciation should have taken place early in their history, then the study adds to the evidence for an adaptive radiation by ecological speciation in Mandarina . However, while the diversity of ecotypes present at each site is dependent on the regime of natural selection and competition, geography still must have an important role.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 88 , 269–282.     

Evidence for ecological speciation in the sister species Candidula unifasciata (Poiret, 1801) and C. rugosiuscula (Michaud, 1831) (Helicellinae, Gastropoda)

This paper studies the speciation of two land snail species in south-east France. By using two mitochondrial and one nuclear gene, the species are shown to be sister species within the larger clade of western European Candidula species. The species never occurred syntopically, but a narrow contact zone population was identified. Recent range expansions inferred from phylogeographical methods indicated that the present day distributions are not limited by the colonization capacity of the species. Analysis of environmental variables suggested distribution along an ecotone. The gastropod community is also correlated to this gradient. Morphometric shell analysis showed that the divergence between the sister species is a result of desiccation-resistant shell characters. We therefore conclude that the cause for the ecological speciation is most probably the establishment of the Mediterranean climate ≈ 3.2 mya. A model of ecological speciation with a moving ecotone is put forward.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 79, 611–628.     

Genome organization in diploid hybrid species of Argyranthemum (Asteraceae) in the Canary Islands

Two diploid species of hybrid origin, Argyranthemum lemsii and A. sundingii , have been described from different valleys in the Anaga peninsula, north-east Tenerife. They have previously been shown to originate from hybridization between the same parental species, the montane A. broussonetii and the coastal A. frutescens , A. broussonetii being the chloroplast donor in one valley and A. frutescens in the other. The specific status of the two hybrid species has been questioned. In this study we used karyotype analysis, FISH, and GISH to address the question of multiple diploid hybrid speciation. GISH did not discriminate clearly between the parental genomes, but differential labelling was observed in separate hybrid populations, indicating different chromosomal rearrangements in different valleys. Small karyotype differences and local loss of rDNA were also observed. Thus separate origins of the same hybrid combination in different valleys in Tenerife have been verified. Our results add some support to the recognition of two species of hybrid origin, but the case serves to illustrate some of the many problems connected with the species concept in plants.  © 2003 The Linnean Society of London, Botanical Journal of the Linnean Society , 2003, 141 , 491–501.     

Plastic resource polymorphism: effects of resource availability on Arctic char (Salvelinus alpinus) morphology

Resource polymorphism has been suggested to be a platform for speciation. In some cases resource polymorphism depends on phenotypic plasticity but in other cases on genetic differences between morphotypes, which in turn has been suggested to be the ongoing development of a species pair. Here we study environmentally induced morphological differences in two age classes of Arctic char ( Salvelinus alpinus ) influencing char performance and diet in relation to resource availability. We found that structurally complex habitats with relatively lower zooplankton densities gave rise to individuals with a deeper body, and a downward positioned tip of the snout compared with individuals from structurally simple habitats with relatively higher zooplankton densities for both age classes. Environment also had an effect on foraging efficiency on zooplankton, with fish from structurally simple habitats had a higher foraging rate than fish from structurally complex habitats. Diet analyses showed that resource use in char mainly depends on the relative abundance of different resources. Therefore, to gain further understanding of resource polymorphism we suggest that future studies must include population dynamic feedbacks by the resources on the consumers.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 85 , 341–351.     

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.     

Paeonia (Paeoniaceae) in the Caucasus

The taxonomy of the genus Paeonia in the Caucasus has been controversial, with recognized species varying in number from one to 13. The taxonomic history of Paeonia in this area is reviewed (including an analysis of the characters used by previous authors) based on extensive field observations, population sampling and critical examination of a large number of herbarium specimens. The results show that Paeonia may be divided into three groups. The P. intermedia group is known from only a single population. In the P. tenuifolia group, all the characters used for distinguishing the three previously recognized species were found to be polymorphic. In the P. daurica group, petal colour, shape and size of leaflets, and indumentum of leaflets and carpels were used to distinguish nine species, but these characters were found to be polymorphic or continuous in variation, and thus can only be used for infraspecific classification. Thus, three species are recognized: P. intermedia , P. tenuifolia and P. daurica . The last species is further divided into five subspecies: sspp. coriifolia , wittmanniana , mlokosewitschii , macrophylla and tomentosa stat. nov .  © 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 143 , 135–150.     

Replicated shape variation between simple and complex habitats in two estuarine fishes

A replicated pattern of habitat‐associated morphology among different lineages may represent adaptive convergence. Deviation from the replicated (shared) pattern of diversification reflects unique (e.g. species specific) effects resulting from site‐ or species‐specific selection, intrinsic factors (e.g. G matrix differences) or chance historical events (e.g. genetic drift). For two distantly‐related estuarine fishes [Lagodon rhomboides (Sparidae; Linnaeus) and Leiostomus xanthurus (Sciaenidae; Lacepède)], we examined shared and unique instances of body shape variation between seagrass (complex) and sand (simple) microhabitats at four sites. We found extensive shape variation between microhabitats for both species. As a shared response, both species from sand had subterminal snouts and long caudal peduncles, whereas those from seagrass had terminal snouts and deep bodies. Unique responses involved a greater difference in Lagodon rhomboides head shape between microhabitats compared to L. xanthurus. Patterns of shape variation fit ecomorphological predictions for foraging in the respective microhabitats (simple versus complex) because deep bodies are expected for fish that must negotiate complex habitats and subterminal snouts facilitate benthic foraging common in barren habitats. Parallel differentiation between microhabitats simultaneously suggests that individuals of each species use a particular microhabitat within estuaries for development and the differentiation in shape represents adaptive convergence. Spatial variation in the magnitude of shape differences between microhabitats was an unexpected finding and suggests that phenotypic variation operates at multiple scales within estuaries. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 147–158.     

A morphometric study on morphological plasticity of shell form in crevice-dwelling Pterioida (Bivalvia)

Relative warp analysis and eigenshape analysis were used to explore the patterns of variation of erratic shell shapes in and among six species of crevice-dwelling pterioid bivalves. The results of morphometric analyses revealed that a great deal of the variance of shell shape within each species can be reduced into principal components which display patterns of variation common to all species examined. In the species with striking variability, a few sets of principal components account for most of the variance of shell shape. On the other hand, in the species lacking considerable variability, several components contribute to form a given variety. Comparison of relative warp and eigenshape scores with centroid sizes indicates that the direction of ontogenetic shape change has been modified through evolution to produce adaptations to habitats such as crevices or the undersides of rocks.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 79, 285–297.     

Genetic and morphological differentiation patterns between sister species: the case of Onthophagus taurus and Onthophagus illyricus (Coleoptera, Scarabaeidae)

The present study investigated the morphological and genetic differentiation pattern between two sympatric dung beetle sister species, Onthophagus taurus and Onthophagus illyricus . The geometric morphometric approach coupled with the use of molecular markers allowed examination of the nature of interspecific relationships and an outline of the evolutionary and geographical processes that might have led to interspecific differentiation and the present-day partial sympatric and syntopic pattern of distribution. Geometric morphometrics failed to discrimininate the two species on the ground of external morphological traits, but revealed interspecific differences when the shape of the primary sexual traits was taken into account. The use of two different molecular markers (cytochrome oxidase subunit I gene and amplified fragment-length polymorphism) demonstrates that the two species are genetically well differentiated, forming two distinguishable lineages probably diverged during the Pliocene by allopatric speciation. No evidence of past or recent introgression and no support for hybridization were found, suggesting that sympatry was established subsequently, when speciation was accomplished. Both molecular markers and genital shape indicate that phenotypically intermediate individuals, despite their ambiguous appearance, are members of O. illyricus species rather than hybrids.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 197–211.     

Experimental evidence for adaptive phenotypic plasticity in a rock-dwelling cichlid fish from Lake Victoria

We demonstrate adaptive phenotypic plasticity (PP) in Neochromis greenwoodi , a rock-dwelling haplochromine cichlid from Lake Victoria. Adaptive phenotypic plasticity will enhance the chance of survival and reproduction in changing or novel environments. For rock-dwelling cichlids it may contribute to the success of settlement after migration between rocky outcrops or islands, since newly colonized patches of rock may offer different food regimes and different competitors. In our experiments, we simulated such situations by raising fry on different diets and with different competitors. We chose diet treatments in such a way that we could predict the direction of anatomical changes from functional demands. We expected an indirect effect of interspecific competition: selectively removing one prey-type by the competing species would leave N. greenwoodi with the other. We found the predicted phenotypic responses to food in trophic traits of N. greenwoodi . However, in the current experimental set-up we did not find a differentiating effect of species of competitor. We discuss the possible role of PP in allopatric and sympatric speciation.  © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 77 , 185−192.     

Changes in ventral head width, a discriminating shape factor among African cichlids, can be induced by chronic hypoxia

A massive enlargement of the gill surface proved to be an important factor in the hypoxia survival of young cichlids. Because the heads of cichlids are densely packed with structures related to both feeding and breathing, we hypothesized that the extra space needed for gill enlargement requires such large structural reorganizations that outer head shape is affected. We used a three-dimensional model to describe changes in the outer head shape of cichlids. Broods of cichlids of different phylogenetic lineages, habitats, and trophic specialization were split and raised at either 10% or 80–90% air saturation. Despite the above-mentioned differences between the species that were used, all hypoxia raised groups showed similar volume enlargements. Volume increases were most prominent in the ventral suspensorial and ventral opercular subcompartments. A relation with the enlarged gills of hypoxia raised fish is likely because the gills are mainly located in these compartments. The differences in ventral width correspond to those found in other studies comprising a wide variety of genotypic and phenotypic variations. The present study shows that such variation in the ventral width is conceivable by phenotypic plasticity alone.   © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 608–619.     

Microsporogenesis and meiotic abnormalities in the hybrid complex of Phlomis composita (Lamiaceae)

The extent of chromosome structural differences such as permanent translocations and paracentric inversions has been studied in the hybrid complex of Phlomis composita and its putative parental taxa P. lychnitis and P. crinita . They are detected as meiotic abnormalities during microsporogenesis. In total, 117 plants from 19 populations in Andalusia (southern Spain) and Levante (eastern Spain) were studied for ploidy level, chromosome clumping, multivalent or univalent formation, late bivalent disjunction with bridges, chromatin bridges and fragments, irregular polysporads and variable pollen size. All individuals had the diploid chromosome number 2 n  = 20, with no significant difference in the frequencies of the above meiotic abnormalities either at taxon or population levels. However, very different frequencies were observed on the regional scale between populations in Andalusia and Levante. The results are discussed within the theoretical framework of homoploid hybrid or recombinational speciation.  © 2003 The Linnean Society of London, Botanical Journal of the Linnean Society , 2003, 143 , 79−85.     

Geographical and morphological variation within and between colour phases in Coris julis (L. 1758), a protogynous marine fish

The possible differences between sexes in patterns of morphological variation in geographical space have been explored only in gonochorist freshwater species. We explored patterns of body shape variation in geographical space in a marine sequential hermaphrodite species, Coris julis (L. 1758), analyzing variation both within and between colour phases, through the use of geometric morphometrics and spatially‐explicit statistical analyses. We also tested for the association of body shape with two environmental variables: temperature and chlorophyll a concentration, as obtained from time‐series of satellite‐derived data. Both colour phases showed a significant morphological variation in geographical space and patterns of variation divergent between phases. Although the morphological variation was qualitatively similar, individuals in the initial colour phase showed a more marked variation than individuals in the terminal phase. Body shape showed a weak but significant correlation with environmental variables, which was more pronounced in primary specimens. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 148–162.     

Intraspecific variation in Anolis sagrei mirrors the adaptive radiation of Greater Antillean anoles

Anolis lizards of the Greater Antilles represent one of the classic examples of vertebrate adaptive radiation. The same morphological types ('ecomorphs') have evolved repeatedly in response to similar ecological pressures on different islands. We tested whether patterns of within species diversification were congruent with between species patterns and the processes leading to the adaptive radiation of Greater Antillean anoles by measuring variation in performance-related morphological characters in the brown anole, Anolis sagrei . We measured morphological and genetic variation in two different habitat types on each of five islands in the Bahamas. We estimated population structure and rates of gene flow within and among islands using eight microsatellite markers. Intraspecific variation in performance-related morphological characters was similar to the pattern of interspecific variation that characterizes the adaptive radiation of this group in the Greater Antilles. For example, limb length was correlated with perch diameter within A. sagrei as has also been shown among species of anole. Morphological divergence in traits has occurred despite relatively high levels of gene flow both within and among islands. These results are discussed in the context of the divergence-with-gene-flow model of speciation. The results provide important intraspecific evidence that the diversification of anoles has been shaped by natural selection and show how ecologically-based selection pressures explain diversification at both the population and species levels.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 189–199.