Morphological Character Displacement Research Articles

Cryptic diversity of limestone karst inhabiting land snails (Cyclophorus spp.) in northern Vietnam, their evolutionary history and the description of four new species.

Limestone karsts can form terrestrial habitat islands for calcium-dependent organisms. In Vietnam, many karst habitats are threatened, while their rich biodiversity is still far from being thoroughly explored. Given that conservation of karst biota strongly relies on correct species identification, the presence of undetected cryptic species can pose severe problems. The present study focuses on cryptic diversity among karst-inhabiting land snails of the genus Cyclophorus in northern Vietnam, where specimens with a similar shell morphology have been reported from various regions. In order to examine the diversity and evolutionary history of this “widespread morphotype”, we generated a Bayesian phylogeny based on DNA sequence data. Automatic Barcode Gap Discovery (ABGD) and the Bayesian implementation of the Poisson tree processes model (bPTP) contributed to species delimitation and analyses of shell shape and size aided the morphological characterisation of individual species. We found that the examined specimens of the widespread morphotype did not form a single monophyletic group in the phylogeny but clustered into several different clades. We delimited nine different species that develop the widespread morphotype and described four of them as new. Processes of convergent evolution were probably involved in the origin of the delimited species, while their generally allopatric distribution could result from interspecific competition. Our findings indicate ongoing processes of speciation and a potential case of morphological character displacement. The high degree of morphological overlap found among the species underlines the importance of DNA sequence data for species delimitation and description in the genus Cyclophorus. Given the findings of the present study and the high potential that as yet undiscovered cryptic taxa have also evolved in other groups of karst-inhabiting organisms, we argue for a systematic and efficient detection and description of Vietnam’s karst biodiversity to provide a solid basis for future conservation planning.

Ecological speciation in darkness? Spatial niche partitioning in sibling subterranean spiders (Araneae : Linyphiidae : Troglohyphantes)

Speciation in subterranean habitats is commonly explained as the result of divergent selection in geographically isolated populations; conversely, the contribution of niche partitioning in driving subterranean species diversification has been rarely quantified. The present study integrated molecular and morphological data with a hypervolume analysis based on functional traits to investigate a potential case of parapatric speciation by means of niche differentiation in two sibling spiders inhabiting contiguous subterranean habitats within a small alpine hypogean site. Troglohyphantes giachinoi, sp. nov. and T. bornensis are diagnosed by small details of the genitalia, which are likely to be involved in a reproductive barrier. Molecular analysis recovered the two species as sister, and revealed a deep genetic divergence that may trace back to the Messinian (~6 million years ago). The hypervolume analysis highlighted a marginal overlap in their ecological niches, coupled with morphological character displacement. Specifically, T. giachinoi, sp. nov. exhibits morphological traits suitable for thriving in the smaller pores of the superficial network of underground fissures (Milieu Souterrain Superficiel, MSS), whereas T. bornensis shows a greater adaptation to the deep subterranean habitat. Our results suggest that different selective regimes within the subterranean environment, i.e. deep caves v. MSS, may either drive local speciation or facilitate contiguous distributions of independently subterranean adapted species.

A new cryptic species of the genus Eleutherodactylus (Amphibia: Anura: Eleutherodactylidae) from Cuba

The widely distributed grass frog of Cuba, Eleutherodactylus varleyi, is shown here to comprise two species. One, E. var-leyi, occurs in western and central Cuba while the other, E. feichtingeri n. sp., occurs in central and eastern Cuba. The twospecies are sympatric in central Cuba, and syntopic in the vicinity of Sierra de Cubitas, Camagüey Province. A molecularphylogeny of mitochondrial DNA sequences from 18 localities confirms the existence of two well-supported major cladescorresponding to each of these species, and the sympatry of the species. Tympanum size and advertisement call are themost useful diagnostic characters, although the two species are shown to have karyotypic differences as well. Possible character displacement in morphology and vocalization, in the area of sympatry, is discussed.

Distribution and Morphological Variation of Microcebus spp. Along an Environmental Gradient in Southeastern Madagascar

The lemurs of Madagascar are known for their extraordinary levels of speciation. However, the mechanisms and environmental conditions that led to this diversity remain obscure. We used 3 species of Microcebus (M. griseorufus, M. murinus, M. rufus) occurring along an environmental gradient as a model to investigate 1) how the different species are distributed in relation to variation in environmental conditions and ecotones; 2) whether or not the morphology of a given species varies in relation to environmental conditions; and 3) whether or not there is evidence for morphological character displacement to reduce congeneric competition in sympatry vs. allopatry. The 3 species of Microcebus show clear associations with specific habitat types. Distributions overlap at ecotones. Nevertheless, the ecotone between dry spiny and gallery forest represents a species boundary between Microcebus griseorufus and M. murinus while the ecotone between dry spiny forest and evergreen humid forest represents the species boundary between M. murinus and M. rufus. Different ambient conditions are not reflected in changes in body measurements of Microcebus murinus living in different vegetation formations. There is no indication for character displacement in sympatry vs. allopatry. Thus, differences in body mass or other morphological characteristics do not contribute to species separation between Microcebus griseorufus and M. murinus. The results confirm the importance of ecotones as species boundaries as a condition postulated for the radiation of lemur and other species on Madagascar. They also demonstrate different habitat affinities of seemingly very similar lemur species and thus illustrate our very limited understanding of the actual selection pressures, adaptations of lemurs to their environments, and their possible response to interspecific competition.

Niche partitioning and species coexistence in a Neotropical felid assemblage

Carnivores have been used as a model to understand the effects of competition in community structure. Behavioral mechanisms that facilitate species coexistence have been poorly explored and may explain the lack of community-wide morphological character displacement in some carnivore assemblages. We use the results of large-scale and intensive camera-trap surveys conducted in the Atlantic Forest of NE Argentina between 2003 and 2008 to describe the spatial patterns of detection and the daily pattern of records of the six wild cat species present in the region (jaguar Panthera onca, puma Puma concolor, ocelot Leopardus pardalis, jaguarundi Puma yagouaroundi, margay Leopardus wiedii, and oncilla Leopardus tigrinus). We use these patterns to generate hypotheses about behavioral differences that may facilitate species coexistence. The larger species were more frequently recorded in the better-protected areas, probably as a result of anthropogenic effects (poaching of cats and their prey). Competitive release from ocelots and jaguarundis may explain why the oncilla and the margay showed the opposite pattern. Morphologically similar species had the most contrasting activity patterns: the margay was exclusively nocturnal and the jaguarundi diurnal. The other species were cathemeral, but alternated their peaks of activity in relation to the relative order of their body weights. The contrasting temporal patterns observed and the ability of pumas and oncillas to adjust their activity patterns to local conditions may facilitate the coexistence of these cat species and explain the lack of character displacement in this assemblage.

Morphological convergence and coexistence in three sympatric North American species of Microtus (Rodentia: Arvicolinae)

AbstractAim Niche theory predicts that ecologically identical species cannot stably coexist in local communities. My aim was to investigate morphological diversity as a possible factor enabling the coexistence of a species‐rich Microtus (Rodentia: Arvicolinae) fauna in a hotspot of North American mammalian diversity, the Greater Yellowstone Ecosystem (GYE).Location The Greater Yellowstone Ecosystem, North America.Methods Using in‐hand morphological measurements of size and shape, I compared the morphologies of three North American vole species (Microtus spp.), in sympatry in the GYE and in allopatry across their ranges, in order to examine: (1) whether morphologies are fixed or plastic and (2) the degree of morphological character displacement or convergence in sympatric species.Results Support was found for plasticity of morphology for all three vole species: M. longicaudus, M. montanus and M. pennsylvanicus. However, Microtus individuals of all species from the GYE area of sympatry were more similar to each other than to allopatric individuals of the same species.Main conclusions Competition among these congeners is not manifested in morphological overdispersion. The response of these congeneric species to the same local ecological conditions is convergent. The relative strength of environmental conditions appears to be stronger than the strength of competitive interactions among the study species.

Geographic morphological variation in parapatric Western Palearctic tree frogs, Hyla arborea and Hyla savignyi: are related species similarly affected by climatic conditions?

Tree frogs Hyla arborea and Hyla savignyi are similar, closely-related species distributed in Europe and the Middle East. We investigated geographic variation in body shape within and between these species, and tested its relationships to macroclimatic conditions. We used morphometric distances (based on size corrected external measurements) to construct phenetic trees (unweighted pair-group method of arithmetical averages, Neighbour-joining), and to test correlations between morphology, geography, and climate by the partial Mantel test. Regardless of their specific affiliation, the parapatric populations of both species from the eastern Mediterranean, where they occupy comparable habitats, are closer to each other in morphospace than to conspecific populations from distal regions. This local interspecific similarity is probably driven by the common response to environment, expressed here as macroclimatic conditions. In support, the geographically close but ecologically vicariant populations of both species from the Caucasus region differ quite substantially in body shape. We suggest that climate-provoked phenotypic variation in closely-related parapatric species should be taken into account as a potential complication to character displacement in morphology. Contrariwise, morphological diversification between related species or their populations could be enhanced by habitat shifts resulting in occupation of different environmental space. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95, 539–556.

Apparent ‘sympatric’ speciation in ecologically similar herbivorous beetles facilitated by multiple colonizations of an island

Coexistence of recently diverged and ecologically similar sister species in complete sympatry represents a particularly compelling case for sympatric speciation. This study investigates the possible sympatric origin of two coexisting bark beetle taxa that utilize the same host plant on the island of La Palma in the Canary Islands. Aphanarthrum subglabrum and Aphanarthrum glabrum ssp. nudum breed inside dead twigs of Euphorbia lamarckii plants and are closely related to the allopatric A. glabrum ssp. glabrum in Tenerife, El Hierro and La Gomera. We tested the various speciation hypotheses in a genealogical context, using mitochondrial gene fragments from Cytochrome Oxidase I and 16S, and nuclear gene fragments from Enolase, Elongation Factor 1alpha and Histone H3. Phylogenetic analyses of the combined nuclear DNA data strongly supported a sister relationship between two sympatric and reproductively isolated taxa in La Palma. However, network analyses of subdivided nonrecombinant segments of the Enolase locus indicated a closer relationship between the two allopatric A. glabrum subspecies, suggesting multiple colonizations of this island. A bimodal distribution of mtDNA haplotypes in La Palma further documented the independent colonization of this island, with asymmetric introgression of mtDNA between two lineages. Consequently, the sympatric origin of the La Palma species is concluded to have involved allopatric phases before the parallel colonization of this island and subsequent introgression at some loci. The clear genetic and morphological evidence for reproductive isolation between these species suggests that the sympatric completion of divergence was either due to initial genetic incompatibility, morphological character displacement in male genitalia, or a combination of these factors.

Character Displacement in Giant Rhinoceros Beetles

I quantitatively analyzed male morphology of two closely related rhinoceros beetles species (Chalcosoma caucasus F. and Chalcosoma atlas L.) in 12 allopatric and seven sympatric locations throughout Southeast Asia. The qualitative features and the magnitude of intraspecific variation of each species were unaltered between allopatric and sympatric locations. Across allopatric locations, body size, horn size, dimorphic dimension, and genitalia size nearly completely overlapped between C. caucasus and C. atlas. Yet, in all sympatric locations, the differences between the two species in these characters were highly significant. While the enlarged difference between the two species in body size in sympatry could be attributed to habitat differentiation, that in genitalia size far exceeded what was expected from the general body-size displacement. These results indicate that morphological character displacement in sympatry was most complete in sexual organs. This may account for the process of existing species conserving themselves as integrated units by avoiding interspecific competition and enhancing reproductive isolation.

Character Displacement in Giant Rhinoceros Beetles

I quantitatively analyzed male morphology of two closely related rhinoceros beetles species (Chalcosoma caucasus F. and Chalcosoma atlas L.) in 12 allopatric and seven sympatric locations throughout Southeast Asia. The qualitative features and the magnitude of intraspecific variation of each species were unaltered between allopatric and sympatric locations. Across allopatric locations, body size, horn size, dimorphic dimension, and genitalia size nearly completely overlapped between C. caucasus and C. atlas. Yet, in all sympatric locations, the differences between the two species in these characters were highly significant. While the enlarged difference between the two species in body size in sympatry could be attributed to habitat differentiation, that in genitalia size far exceeded what was expected from the general body‐size displacement. These results indicate that morphological character displacement in sympatry was most complete in sexual organs. This may account for the process of existing species conserving themselves as integrated units by avoiding interspecific competition and enhancing reproductive isolation.

CHARACTER DISPLACEMENT IN AUSTRALIAN DASYURID CARNIVORES: SIZE RELATIONSHIPS AND PREY SIZE PATTERNS

The four different assemblages of marsupial dasyuroid carnivores in Australia, comprising four species on the island of Tasmania and three different two-species assemblages on the mainland of Australia, present an ideal opportunity to test the theories of competitively based morphological character displacement. With males and females treated as separate morphospecies, four trophic characters that relate to killing and feeding behavior and skull length, as a measure of body size, were examined for evidence of morphological patterning, latitudinal size variation, and sexual dimorphism. The competitive basis for character displacement in intra- and interspecific variation in prey size was sought from dietary analysis at a field site. Even spacing in canine strength, but not in other characters, was found among species and sexes of quolls (Dasyurus viverrinus and D. maculatus), but not including the devil (Sarcophilus laniarius) or the thylacine (Thylacinus cynocephalus), in Tasmania. Even spacing was found in temporalis muscle size for all combinations of the four Tasmanian species. Canine breaking strength and muscle strength driving the canines can be construed as the most important trophic characters involved in prey capture, and therefore in determining the upper size of prey that can be handled. Even spacing was found in Tasmania, where there are two larger species in the guild, but not in any of the three mainland assemblages where the larger species of carnivores have been absent for many generations. The basis for the observed morphological patterning in killing behavior, evidence for even spacing in prey size, and partial character release on the mainland are consistent with the hypothesis of competitive character displacement. These size relationships result from a complex interplay of factors. Latitudinally correlated size variation has influenced an increase in body size and canine strength in D. viverrinus and an increase in body size in D. maculatus in Tasmania. This is countered by decreased canine strength in D. maculatus in Tasmania resulting from competitive character displacement. The result is character convergence. Sexual selection also influences size relationships.

Character Displacement in Australian Dasyurid Carnivores: Size Relationships and Prey Size Patterns

The four different assemblages of marsupial dasyuroid carnivores in Australia, comprising four species on the island of Tasmania and three different two-species assemblages on the mainland of Australia, present an ideal opportunity to test the theories of competitively based morphological character displacement. With males and females treated as separate morphospecies, four trophic characters that relate to killing and feeding behavior and skull length, as a measure of body size, were examined for evidence of morphological patterning, latitudinal size variation, and sexual dimorphism. The competitive basis for character displacement in intra- and interspecific variation in prey size was sought from dietary analysis at a field site. Even spacing in canine strength, but not in other characters, was found among species and sexes of quolls (Dasyurus viverrinus and D. maculatus), but not including the devil (Sarcophilus laniarius) or the thylacine (Thylacinus cynocephalus), in Tasmania. Even spacing was found in temporalis muscle size for all combinations of the four Tasmanian species. Canine breaking strength and muscle strength driving the canines can be construed as the most important trophic characters involved in prey capture, and therefore in determining the upper size of prey that can be handled. Even spacing was found in Tasmania, where there are two larger species in the guild, but not in any of the three mainland assemblages where the larger species of carnivores have been absent for many generations. The basis for the observed morphological patterning in killing behavior, evidence for even spacing in prey size, and partial character release on the mainland are consistent with the hypothesis of competitive character displacement. These size relationships result from a complex interplay of factors. Latitudinally correlated size variation has influenced an increase in body size and canine strength in D. viverrinus and an increase in body size in D. maculatus in Tasmania. This is countered by decreased canine strength in D. maculatus in Tasmania resulting from competitive character displacement. The result is character convergence. Sexual selection also influences size relationships.

EVIDENCE FOR ECOLOGICAL CHARACTER DISPLACEMENT IN WESTERN AMERICAN CATOSTOMID FISHES.

Much of recent ecological theory rests on assumption that primary factor responsible for organization of natural communities, particularly of animals, is interspecific competition (e.g., MacArthur, 1972; Schoener, 1975). The validity of this assumption depends almost exclusively on inference drawn from observational evidence of two types. Morphological changes in form of ecological character displacement (Brown and Wilson, 1959; Grant, 1972) and niche shifts correlated with geographic variation in number or density of closely related species are generally considered strongest available evidence for importance of interspecific competition (MacArthur, 1972; Cody, 1974; Schoener, 1974, 1975). Grant (1972, 1975) defines ecological character displacement to be the process by which a morphological character state of a species changes under natural selection arising from presence, in same environment, of one or more species similar to it ecologically . By this definition Grant would include both character convergence and divergence but would exclude cases of changes in character state due to related process of character release. It seems clear that interspecific interaction implicit in Grant's (1972, 1975) definition of ecological character displacement is competition. Furthermore, this causal relationship must be demonstrated if ecological character displacement is to be used as observational evidence for occurrence of interspecific competition. Therefore, we define competitive character displacement to be a change of character state in a population that is due to natural selection arising as a result of competition with individuals of another population in same environment. The characters may be morphological, ecological, behavioral, or physiological and change may be either divergent or convergent. By divergent competitive character displacement we mean that a character state of a population in ecological sympatry (=syntopy, Rivas, 1964) exhibits greater difference than is case when allopatric populations are contrasted, and that this effect can be attributed to sympatry. If contrast of allopatric and sympatric populations reveals that character states of two populations are more similar in areas of sympatry than in areas of allopatry and if this effect can be attributed to competition, then situation is one of convergent character displacement. Ecological theory predicts those situations in which convergent or divergent displacement would be expected (MacArthur and Levins, 1964, 1967; MacArthur and Wilson, 1967; Schoener, 1969a, 1969b, 1970; MacArthur, 1972). In all of these models selection responsible for character state change or niche shift arises as a result of interspecific competition. Grant (1972) in his critical review of evidence for ecological character displacement, concluded that the evidence for ecological aspect of morphological character displacement is weak and that the detection of character displacement in its ecological aspect, particularly in mainland regions, will require a level of detail that has so far not been produced in a single study. The weakness of available evidence for competitive character displacement lies in difficulty of establishing unambiguously that character state of

Ecological Character Displacement in a Lizard

Two species of subterranean skinks ( Typhlosaurus ) are sympatric in part of the southern Kalahari Desert. The geographic range of the smaller species ( T. gariepensis ) is entirely included within that of the larger one ( T. lineatus ). Snout-vent lengths, head dimensions, proportional head lengths, and prey size of T. lineatus are larger in sympatry than in allopatry. Morphological and dietary evidence support the hypothesis that behavioral and morphological character displacement has occurred in female and immature T. lineatus , which reduces dietary overlap with T. gariepensis . Dietary data for male T. lineatus may be conflicting.

Ecological Shifts in Sympatry: Kalahari Fossorial Lizards (Typhlosaurus)

Two species of legless, fossorial skinks (Typhlosaurus) are partially sympatric in the Kalahari Desert. Typhlosaurus lineatus occur both in the sandridge and flatland geographic provinces of the Kalahari, in dune streets and on sandridgesmicrogeographically in sympatry, and primarily under log and leaf litter microhabitats. Typhlosaurus gariepensis, always microgeogrphically, and primarily in basal roots of bunch grass microhabitats. Microhabitat overlap in sympatry is low. Morphologically, T. lineatus differ from T. gariepensis in being longer and in having a longer and wider head. Snout—vent lengths, head dimensions, and proportional head lengths of sympatric T. lineatus are larger than those of allopatric T. lineatus; thus T. lineatus displace from T. gariepensis in sympatry. Both species are viviparous, have one brood per year, and give birth in summer after a 5—mo gestation period. Maturity is reached at minimum ages of one and two—thirds yr. Mean litter size of T. lineatus is 1.6, whereas T. gariepensis have but one young. A response to competition between the two species is suggested by the facts that offspring of sympatric T. lineatus are significantlyheavier than those of allopatric females, and that fewer sympatric T. lineatus females are reproductive than allopatric females. Because Typhlosaurus are termite specialists (92.4% of diet by volume), termitesin guts were identified to species and caste. Compared with sympatric T. lineatus, T. gariepensis eat more Psammotermes workers, fewer Allodontermes major workers, and scarcely any Hodotermes. Sympatric T. lineatus eat fewer Psammotermes workers and more Allodontermes major workers than do allopatric T. lineatus. Prey size differences parallel lizard size differences. Because of dietary shifts by T. lineatus in sympatry, dietary overlap with T. gariepensis is substantially reduced for females and immatures, although not for males. Strong morphological and dietary evidence support, for T. lineatus females and immatures, the hypothesis that behavioral and morphological character displacement has occurred which reduces dietary overlap with T. gariepensis. Dietary data for male T. lineatus are possibly conflicting.

SOME CALANOID COPEPODS FROM ARIZONA WITH NOTES ON CONGENERIC OCCURRENCES OF DIAPTOMUS SPECIES

Seven species of Diaptomus are reported from Arizona, including 4 new to the state. D. shoshone, D. nudus, and D. leptopus occur on the Colorado Plateau; D. clavipes and D. siciloides are abundant in the mountainous area below the Mogollon Rim; D. albuquerquensis occurs rarely in turbid ponds on the Plateau and in the Sonoran Desert; D. dorsalis lives in permanent, oligohaline ponds near Phoenix.Thirty‐four examples of congeneric coexistence are presented, including 3 from Arizona. In 24 instances, coexistence involved species of different subgenera. Differences in length of co‐occurring species are common and are particularly marked in temporary ponds and saline lakes. Genetic changes in the nature of character displacement may modify dimensions of coexisting species, although environmental factors other than congeneric competition also play a part. Adult diaptomids from Arizona tanks may be larger when early instars are passed during summer rather than winter. Extrinsic factors thus tend to blur morphological character displacement. Modified life cycles and ecological displacement are further intrinsic mechanisms whereby habitats are partitioned, although not revealed by ordinary sampling techniques.