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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.

Animals↗

Ecological and life history characteristics predict population genetic divergence of two salmonids in the same landscape.

Ecological and life history characteristics such as population size, dispersal pattern, and mating system mediate the influence of genetic drift and gene flow on population subdivision. Bull trout (Salvelinus confluentus) and mountain whitefish (Prosopium williamsoni) differ markedly in spawning location, population size and mating system. Based on these differences, we predicted that bull trout would have reduced genetic variation within and greater differentiation among populations compared with mountain whitefish. To test this hypothesis, we used microsatellite markers to determine patterns of genetic divergence for each species in the Clark Fork River, Montana, USA. As predicted, bull trout had a much greater proportion of genetic variation partitioned among populations than mountain whitefish. Among all sites, FST was seven times greater for bull trout (FST = 0.304 for bull trout, 0.042 for mountain whitefish. After removing genetically differentiated high mountain lake sites for each species FST, was 10 times greater for bull trout (FST = 0.176 for bull trout; FST = 0.018 for mountain whitefish). The same characteristics that affect dispersal patterns in these species also lead to predictions about the amount and scale of adaptive divergence among populations. We provide a theoretical framework that incorporates variation in ecological and life history factors, neutral divergence, and adaptive divergence to interpret how neutral and adaptive divergence might be correlates of ecological and life history factors.

Animals↗

Rapid lineage accumulation in a non-adaptive radiation: phylogenetic analysis of diversification rates in eastern North American woodland salamanders (Plethodontidae: Plethodon).

Adaptive radiations have served as model systems for quantifying the build-up of species richness. Few studies have quantified the tempo of diversification in species-rich clades that contain negligible adaptive disparity, making the macroevolutionary consequences of different modes of evolutionary radiation difficult to assess. We use mitochondrial-DNA sequence data and recently developed phylogenetic methodologies to explore the tempo of diversification of eastern North American Plethodon, a species-rich clade of woodland salamanders exhibiting only limited phenotypic disparity. Lineage-through-time analysis reveals a high rate of lineage accumulation, 0.8 species per million years, occurring 11-8 million years ago in the P. glutinosus species group, followed by decreasing rates. This high rate of lineage accumulation is exceptional, comparable to the most rapid of adaptive radiations. In contrast to classic models of adaptive radiation where ecological niche divergence is linked to the origin of species, we propose that phylogenetic niche conservatism contributes to the rapid accumulation of P. glutinosus-group lineages by promoting vicariant isolation and multiplication of species across a spatially and temporally fluctuating environment. These closely related and ecologically similar lineages persist through long-periods of evolutionary time and form strong barriers to the geographic spread of their neighbours, producing a subsequent decline in lineage accumulation. Rapid diversification among lineages exhibiting long-term maintenance of their bioclimatic niche requirements is an under-appreciated phenomenon driving the build-up of species richness.

Animals↗

Homoploid Hybrid Speciation in a Marine Pelagic Fish.

Homoploid hybrid speciation (HHS) is an enigmatic evolutionary process where new species arise through hybridisation of divergent lineages without changes in chromosome number. Although increasingly documented in various taxa and ecosystems, convincing cases of HHS in marine fishes have been lacking. This study presents a possible case of HHS in a pelagic marine fish based on comprehensive genomic, morphological, and ecological analyses. Population genomics, species tree estimation, and tests of introgression and admixture identified three sympatric clusters in Megalaspis cordyla in the western Pacific and the admixed nature of one cluster between the others. Moreover, model-based demographic inference favoured a hybrid speciation scenario over introgression for the origin of the admixed cluster. While contemporary gene flow suggested partial reproductive isolation, examination of occurrence data and ecologically relevant morphological characters suggested ecological differences between the clusters, potentially contributing to the reproductive isolation and niche partitioning in sympatry. The clusters are also morphologically distinguishable and thus can be taxonomically recognised as separate species. The hybrid cluster is restricted to the coasts of Taiwan and Japan, where all three clusters coexist. The parental clusters are additionally found in lower latitudes, where they display non-overlapping distributions. Given the geographical distributions, estimated times of species formation, and patterns of historical demographic changes, we propose that the Pleistocene glacial cycles were the primary driver of HHS in this system. We also develop an ecogeographic model of HHS in marine coastal ecosystems, including a novel hypothesis to explain the initial stages of HHS.

Animals↗

Harmonic-hopping in Wallacea's bats.

Evolutionary divergence between species is facilitated by ecological shifts, and divergence is particularly rapid when such shifts also promote assortative mating. Horseshoe bats are a diverse Old World family (Rhinolophidae) that have undergone a rapid radiation in the past 5 million years. These insectivorous bats use a predominantly pure-tone echolocation call matched to an auditory fovea (an over-representation of the pure-tone frequency in the cochlea and inferior colliculus) to detect the minute changes in echo amplitude and frequency generated when an insect flutters its wings. The emitted signal is the accentuated second harmonic of a series in which the fundamental and remaining harmonics are filtered out. Here we show that three distinct, sympatric size morphs of the large-eared horseshoe bat (Rhinolophus philippinensis) echolocate at different harmonics of the same fundamental frequency. These morphs have undergone recent genetic divergence, and this process has occurred in parallel more than once. We suggest that switching harmonics creates a discontinuity in the bats' perception of available prey that can initiate disruptive selection. Moreover, because call frequency in horseshoe bats has a dual function in resource acquisition and communication, ecological selection on frequency might lead to assortative mating and ultimately reproductive isolation and speciation, regardless of external barriers to gene flow.

Acoustics↗

Population genetics of tandem trypsin inhibitor genes in Arabidopsis species with contrasting ecology and life history.

Duplicated genes are important in the evolution and ecology of plant-defences because herbivore and pathogen attack can be countered via functional diversification at two levels: among duplicated loci and within loci. We explore molecular sequence variation for two members of a defence-related gene family, Arabidopsis thaliana trypsin inhibitors (ATTI), in A. thaliana and a closely related species, A. lyrata subspp. petraea. A worldwide sample of the inbreeding annual A. thaliana had less genetic variation at two ATTI loci (piTOTAL <or= 0.0006) than observed previously at other functional loci. A significant excess of high frequency derived alleles in the signal sequence and 5' UTR of ATTI2 was consistent with a model of positive selection. However, demographic processes such as population subdivision and expansion, both likely to have occurred in A. thaliana during the last 10 000 years, can also give rise to similar deviations from neutrality. A single population of A. lyrata subspp. petraea in Germany had up to an order of magnitude more standing genetic variation at ATTI loci than the species-wide sample of A. thaliana. Although the level of variability for ATTI1 and ATTI2 within this single population was similar to, or even greater than, observed species-wide diversity for other loci in A. lyrata, there was little evidence to reject an equilibrium neutral model. A spatially explicit sample of 87 A. lyrata subspp. petraea individuals detected outbreeding (FIS = -0.16; FIT = -0.15) but little population subdivision (FST = 0.006) in this self-incompatible perennial herb. Genetic differences between Arabidopsis species were consistent with, but not fully explained by, divergence in ecology and life history. Diversification appears to have occurred in different functional domains for the tandemly duplicated ATTI1 and ATTI2 genes; the majority of fixed replacements in ATTI1 surround the enzyme binding site of the mature protein, whereas in ATTI2 most functional evolutionary change is located in the signal peptide. This pattern is consistent with a hypothesis of subfunctionalization in trypsin inhibitory function.

Arabidopsis↗

Molecular biomarkers and adaptation to environmental stress in moon jelly (Aurelia spp.).

We describe a strategy that identifies molecular biomarkers and links the study of abiotic stress to evolutionary history. By utilizing the moon jellyfish Aurelia spp. as a model, we identified genes differentially regulated in response to the chemical stressor tributyltin by means of complementary DNA subtraction analyses. Expression of 3 out of 25 identified candidate genes, one oxidative stress gene, one heat shock (hsp70) gene, and one GTP-binding gene, was quantified under laboratory conditions and in field tests using semiquantitative reverse transcriptase polymerase chain reaction. Differential expression patterns were found following exposure to tributyltin and temperature treatments. The findings suggest that the identified genes are involved in response to chemical as well as heat- induced stress and may serve as biomarkers for monitoring marine habitats. Gene regulatory patterns combined with phylogenetic inferences of the hsp70 gene support a possible role of ecologically driven divergence within the genus Aurelia. We show that added information on genetic variability can raise the predictive power of molecular biomarkers in studies of individual stress response.

Adaptation, Biological↗

Phylogeography of Aglais urticae (Lepidoptera) based on DNA sequences of the mitochondrial COI gene and control region.

Mitochondrial DNA (mtDNA) sequences of the COI gene and the control region were used to examine the genetic population structure of Aglais urticae L. (Lepidoptera) over its entire geographic range, i.e., the Palaearctic. The phylogenetic relationships within and between A. urticae subspecies were determined and patterns of mtDNA divergence and ecological differentiation were compared. High gene flow together with a recent and sudden population expansion characterise the genetic population structure of this species. No geographically induced differentiation was observed, nor were subspecies identified as separate evolutionary units. The discrepancy between the genetic and ecological variation is most likely due to the slower rate of mtDNA evolution compared to ecological differentiation. The control region proved to be a less useful molecular marker for the population genetics and the phylogenetic reconstruction of closely related taxa in A. urticae than it has for other species. The extreme bias in adenine and thymine content (A+T=90.91%) probably renders this region highly susceptible to homoplasy, resulting in a less informative molecular marker.

Animals↗

Comparative analysis of morphological traits among Drosophila melanogaster and D. simulans: genetic variability, clines and phenotypic plasticity.

The two sibling cosmopolitan species, Drosophila melanogaster and D. simulans, are able to proliferate under very different climatic conditions. This has resulted in local adaptations, which are often arranged in latitudinal clines. Such clines are documented for body weight, wing and thorax length, sternopleural and abdominal bristle number, ovariole number and thoracic pigmentation. The overall magnitude of geographical differentiation is, however, much less in D. simulans than in D. melanogaster, and latitudinal clines are less pronounced. The fact that natural populations live under different climates raises the problem of interaction between temperature and phenotype. The reaction norms of morphometrical traits have been investigated as a function of growth temperature. The shapes of the response curves vary according to the investigated trait. They are generally curvilinear and can be described by calculating characteristic values after polynomial adjustments. For a given trait, the reaction norms of the two species are similar in their shape, although some significant differences may be observed. Within each species, significant differences are also observed between geographic populations: reaction norms are not parallel and the divergence is better marked when more distant populations (e.g., temperate and tropical) are compared. It thus appears that besides mean trait value, phenotypic plasticity is also a target of natural selection. A specific analysis of wing shape variation according to growth temperature was also undertaken. Reaction norms with different shapes may be observed in various parts of the wing: the major effect is found between the basis and the tip of the wing, but in a similar way in the two species. By contrast, some ratios, called wing indices by taxonomists, may exhibit completely different reaction norms in the two species. For a single developmental temperature (25 degrees C) the phenotypic variability of morphometrical traits is generally similar in the two species, and also the genetic variability, estimated by the intraclass correlation. A difference exists, however, for the ovariole number which is less variable in D. simulans. Variance parameters may vary according to growth temperature, and a detailed analysis was made on wing dimensions. An increase of environmental variability at extreme, heat or cold temperatures, has been found in both species. Opposite trends were, however, observed for the genetic variability: a maximum heritability in D. simulans at middle temperatures, corresponding to a minimum heritability in D. melanogaster. Whether such a difference exists for other traits and in other populations deserves further investigations. In conclusion, morphometrical analyses reveal a large amount of significant differences which may be related to speciation and to the divergence of ecological niches. Within each species, numerous geographic variations are also observed which, in most cases, reflect some kinds of climatic adaptation.

Animals↗

The role of stochasticity in fungal community assembly: explaining apparent stochasticity with field experiments.

Stochasticity is a main process in community assembly. However, experimental studies rarely target stochasticity in natural communities, and hence experimental validation of stochasticity estimates in observational studies is lacking. Here, we combine experimental and observational data to unravel the role of stochasticity in the assembly of wood-inhabiting fungi. We carried out a replicated field experiment where the natural colonization of a focal fungal species was simulated through inoculation, and the local fungal communities were monitored through DNA metabarcoding before and after the inoculations. The amount of stochasticity in fungal colonization was less pronounced than expected from the amount of unpredictability in observational data, suggesting that stochasticity may play a smaller role in fungal occurrence than previously anticipated, or that it may be a stronger influence in the dispersal and establishment phases than in colonization per se. Stochasticity was more prominent in the initial phase of community succession, with the earliest successional stage involving a higher level of stochasticity than the later stage after 2 years. We conclude that experimentally measuring the role of stochasticity in community assembly is feasible for species-rich communities under natural conditions and highlight the importance of experimentally testing the accuracy of stochasticity estimates based on observational data.

Stochastic Processes↗

The evolution of reproductive isolation in the ectomycorrhizal Hebeloma crustuliniforme aggregate (Basidiomycetes) in northwestern Europe: a phylogenetic approach.

To reconstruct the evolution of reproductive isolation in the ectomycorrhizal Hebeloma crustuliniforme aggregate (Basidiomycetes), phylogenetic relationships were determined between strains that belong to a clade consisting of nine intercompatibility groups (ICGs, biological species). Four of these nine ICGs are partially compatible and belong to the H. crustuliniforme aggregate. Different levels of partial compatibility have been found between these four ICGs. Between ICGs 3 and 4, 15% of the combinations were compatible. One strain was compatible with all isolates of both ICGs 3 and 4 and also with one isolate of ICG 2. Both a nuclear phylogeny, based on ribosomal IGS sequence data, and a mitochondrial phylogeny, based on a group-I intron located in the large subunit ribosomal RNA gene (LrRNA), were reconstructed. The level of incompatibility was compared with the phylogenetic history of individuals belonging to this clade. Different relationships were found between the level of compatibility and the relative age of the most recent common ancestor (MRCA) for different ICGs. On the one hand, the evolution of incompatibility between ICGs 2 and 3/4 is most consistent with the class of "divergence- first" models because a positive correlation was found between the relative age of the MRCA and the level of incompatibility for ICG 2 versus 3/4. On the other hand, the lack of such a correlation for ICGs 3 and 4 shows that (partial) incompatibility between these ICGs has arisen without strong divergence. The ecological (and to a lesser extent geographical) differences found between ICGs 3 and 4 suggest that selection for incompatibility, associated with host tree preference, has been important in the evolution of incompatibility between these two ICGs. The incongruence between the nuclear and mitochondrial trees for ICG 1 could be explained by a hybrid origin of this ICG, with different donors of the mitochondrial and nuclear sequences.

Basidiomycota↗

The evolution of chemoreception in squamate reptiles: a phylogenetic approach.

Recent advances in the field of squamate reptile chemoreception have been paralleled by the growth and preeminence of cladistics in the field of systematics, but for the most part, workers in the former have failed to incorporate the conceptual and informational advances of the latter. In this paper, I attempt a preliminary rapprochement by combining the methods of phylogenetic systematics and current hypotheses of squamate relationships with an overview of squamate chemosensory biology. This purely phylogenetic approach leads to a number of falsifiable generalizations about the evolution of chemoreception in squamates: 1) Evolution of this system is conservative rather than plastic, reflecting to a large extent suprafamilial attributes rather than adaptation to local conditions; 2) Anguimorphs are highly chemosensory and teiids show convergence with this group; 3) Tongue-flicking, a bifurcated tongue tip, a vomeronasal (VNO) mushroom body, and a complete circular muscle system in the tongue are a correlated character complex associated with the attainment, in squamates, of a direct VNO-oral connection and the loss of a VNO-nasal connection; 4) There is little support for a visual-chemosensory dichotomy within Squamata; 5) Gekkotans are allied with Autarchoglossa, both phylogenetically and in terms of chemosensory biology; 6) Iguania are highly variable in chemosensory development; iguanids represent the primitive iguanian condition, while agamids and chamaeleonids have secondarily reduced or lost their chemosensory abilities; 7) Apparent contradictions in chemosensory behavior among iguanids probably represent intrafamilial divergence; 8) Ecological correlates within Iguanidae and other taxa might be spurious, resulting from historical factors unrelated to the adaptations in question; 9) The mechanical demands of lingual food prehension have constrained chemosensory evolution in Iguania; chemosensory evolution within Scleroglossa was permitted by the liberation of the tongue from this ancestral role.

Amphibians↗

Parallel analyses of individual and ecologic data on residential radon, cofactors, and lung cancer in Sweden.

Divergent results from ecologic and analytic studies on residential radon and lung cancer have created uncertainty in terms of risk assessment. The authors performed concurrent analyses on individual and aggregated data from the nationwide case-control study of residential radon and lung cancer in Sweden. For data aggregated on the county level, the ecologic excess relative risk estimates per 100 Bqm(-3) residential radon concentration ranged from -0.03 (95% confidence interval (CI) -0.21 to 0.15) to 0.00 (95% CI -0.21 to 0.21) with different adjustment for cofactors. For individual-level data, the average within-county excess relative risk estimates ranged from 0.07 (95% CI -0.01 to 0.15) to 0.11 (95% CI 0.01-0.27) with similar adjustment. Effect modification by differential county-level radon-smoking correlations appeared insufficient as an explanation for ecologic bias in the Swedish data. On the other hand, adjustment for latitude led to congruence between the two levels of analysis. The results confirm that ecologic studies may be misleading in studies of weak associations, even when major risk factors are accounted for. The large impact of latitude may be unique to Sweden and due to the correlation of latitude both with residential radon and other determinants of lung cancer risk.

Adult↗

Refugial isolation versus ecological gradients. Testing alternative mechanisms of evolutionary divergence in four rainforest vertebrates.

Hypotheses for divergence and speciation in rainforests generally fall into two categories: those emphasizing the role of geographic isolation and those emphasizing the role of divergent selection along gradients. While a majority of studies have attempted to infer mechanisms based on the pattern of species richness and congruence of geographic boundaries, relatively few have tried to simultaneously test alternative hypotheses for diversification. Here we discuss four examples, taken from our work on diversification of tropical rainforest vertebrates, in which we examine patterns of genetic and morphological variation within and between biogeographic regions to address two alternative hypotheses. By estimating morphological divergence between geographically contiguous and isolated populations under similar and different ecological conditions, we attempt to evaluate the relative roles of geographic isolation and natural selection in population divergence. Results suggest that natural selection, even in the presence of appreciable gene flow, can result in morphological divergence that is greater than that found between populations isolated for millions of years and, in some cases, even greater than that found between congeneric, but distinct, species. The relatively small phenotypic divergence that occurs among long-term geographic isolates in similar habitats suggests that morphological divergence via drift may be negligible and/or that selection is acting to produce similar phenotypes in populations occupying similar habitats. Our results demonstrate that significant phenotypic divergence: (1) is not necessarily coupled with divergence in neutral molecular markers; and (2) can occur without geographic isolation in the presence of gene flow.

Adaptation, Biological↗

Testing alternative explanations of character shifts against ecological character displacement in brook sticklebacks (Culaea inconstans) that coexist with ninespine sticklebacks (Pungitius pungitius).

Ecological character displacement (ECD) provides opportunities to test how resource competition generates diversifying selection that results in adaptive divergence. We quantify an association between phenotypic and ecological divergence between two similar small fishes, brook (Culaea inconstans) and ninespine (Pungitius pungitius) sticklebacks, in replicate northern Ontario lakes, Canada. The two species partition resources and habitat, where they coexist, and brooks that coexist with ninespines are more benthically specialized in body form and diet than brooks from local allopatric populations. Here we test various explanations for this pattern. Chance is unlikely to have been the primary cause because divergence is replicated in three separate populations. Preliminary comparisons indicate that resource availability and a variety of abiotic ecological conditions are generally similar between sympatric and allopatric sites, and so do not readily account for the divergence. Biased colonization or extinction is less likely to account for the divergence because character values in sympatry tend to exceed those in allopatry, as expected if they have repeatedly evolved under diversifying selection. Recent studies have also demonstrated that these two species compete, and that competitive effects are more severe for allopatric compared to sympatric brook forms, as predicted if divergence reflects the ghost of competition past. Ongoing studies indicate heritable variation in this system. Our results suggest that even small amounts of character shifts can influence competition and hence relative fitness, further implicating a role for ECD in the evolution of biodiversity.

Animals↗

Adaptive divergence and the evolution of reproductive isolation in the wild: an empirical demonstration using introduced sockeye salmon.

Populations exposed to different ecological environments should diverge for phenotypic traits that influence survival and reproduction. This adaptive divergence should reduce gene flow between populations because immigrants become less fit than residents and because hybrids perform poorly in either environment (i.e., ecologically-dependent reproductive isolation). Here I demonstrate adaptive divergence and the evolution of reproductive isolation in populations of sockeye salmon (Oncorhynchus nerka) introduced from a common ancestral source into a new lake system (Lake Washington, Washington). The introduced fish founded several new populations, two of which experience very different environments during breeding and early development (Cedar River v.s. Pleasure Point beach). Over 13 generations, the two populations diverged for adult traits (female body size, male body depth; measured in the wild) and embryo traits (survival to hatching, development rate, size at emergence; measured in a common environment). The rates of divergence for these characters were similar to those observed in other examples of 'rapid evolution', and can best be attributed to natural selection. Partial reproductive isolation has evolved in concert with adaptive divergence: the rate of exchange of adults between the populations (determined using natural tags) is higher than the rate of gene flow (determined using DNA microsatellites). The demonstration that adaptive divergence can initiate reproductive isolation in less than 13 generations suggests that the first signs of 'ecological speciation' may appear soon after new environments are first colonized.

Adaptation, Biological↗

What are bacterial species?

Bacterial systematics has not yet reached a consensus for defining the fundamental unit of biological diversity, the species. The past half-century of bacterial systematics has been characterized by improvements in methods for demarcating species as phenotypic and genetic clusters, but species demarcation has not been guided by a theory-based concept of species. Eukaryote systematists have developed a universal concept of species: A species is a group of organisms whose divergence is capped by a force of cohesion; divergence between different species is irreversible; and different species are ecologically distinct. In the case of bacteria, these universal properties are held not by the named species of systematics but by ecotypes. These are populations of organisms occupying the same ecological niche, whose divergence is purged recurrently by natural selection. These ecotypes can be discovered by several universal sequence-based approaches. These molecular methods suggest that a typical named species contains many ecotypes, each with the universal attributes of species. A named bacterial species is thus more like a genus than a species.

Bacteria↗

Deep molecular divergence in the absence of morphological and ecological change in the Californian coastal dune endemic trapdoor spider Aptostichus simus.

Aptostichus simus is a trapdoor spider endemic to the coastal dunes of central and southern California and, on morphological grounds, is recognized as a single species. Mitochondrial DNA 16S rRNA sequences demonstrate that most populations are fixed for the same haplotype and that the population haplotypes from San Diego County, Los Angeles County, Santa Rosa Island, and Monterey County are extremely divergent (6-12%), with estimated separation times ranging from 2 to 6 million years. A statistical cluster analysis of morphological features demonstrates that this genetic divergence is not reflected in anatomical features that might signify ecological differentiation among these lineages. The species status of these divergent populations of A. simus depends upon the species concept utilized. If a time-limited genealogical perspective is employed, A. simus would be separated at the base into two genetically distinct species. This study suggests that species concepts based on morphological distinctiveness, in spider groups with limited dispersal capabilities, probably underestimate true evolutionary diversity.

Animals↗