The tree, the network, and the species

To enrich the Hennigian internodal conception of species, a new formalization of the definition of the species concept is proposed. This rigorous definition allows for considerable unification of the various, and sometimes conflicting, techniques of species delimitation used in practice. First, the domain of such a definition is set out, namely, the set of all organisms on Earth, past, present, and future. Next, the focus is on the genealogical relationship among organisms, which provides the key to analysing the giant or global genealogical network (GGN) connecting all these organisms. This leads to the construction of an algorithm revealing the topological structure of the GGN, from families to lineages, ending up with a definition of species as equivalence classes of organisms corresponding to branches of the 'tree of life'. Such a theoretical definition of the species concept must be accompanied by various recognition criteria to be operational. These criteria are, for example, the ill-named 'biological species concepts', 'phylogenetic species concepts', etc., usually, but wrongly, presented as definitions of the species concept. Besides clarifying this disputed point, the definition in the present study displays the huge diversity of the scales (time-scale and population size) involved in actual species, thus explaining away the classical problems raised by previous attempts at defining the species concept (uniparental reproduction, temporal depth of species, and hybridization).  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 509–521.     

Recognizing species,present and past

Nobody disputes that nature is meaningfully “packaged” in some way. But debate persists over exactly how (and even whether) the boundaries dividing taxa should (can) be drawn. At one end of the scale, some zealots abstrusely deny real existence to higher taxa.¹ At the other, laborers at the taxonomic rock‐face confront genuine challenges in recognizing and delineating the species that systematists agree constitute the most fundamental unit of taxonomic analysis. 2 , 3     

Progress toward a general species concept

New insights in the speciation process and the nature of "species" that accumulated in the past decade demand adjustments of the species concept. The standing of some of the most broadly accepted or most innovative species concepts in the light of the growing evidence that reproductive barriers are semipermeable to gene flow, that species can differentiate despite ongoing interbreeding, that a single species can originate polyphyletically by parallel evolution, and that uniparental organisms are organised in units that resemble species of biparental organisms is discussed. As a synthesis of ideas in existing concepts and the new insights, a generalization of the genic concept is proposed that defines species as groups of individuals that are reciprocally characterized by features that would have negative fitness effects in other groups and that cannot be regularly exchanged between groups upon contact. The benefits of this differential fitness species concept are that it classifies groups that keep differentiated and keep on differentiating despite interbreeding as species, that it is not restricted to specific mutations or mechanisms causing speciation, and that it can be applied to the whole spectrum of organisms from uni- to biparentals.     

Three new species of Stiphrornis (Aves: Muscicapidae) from the Afro-tropics,with a molecular phylogenetic assessment of the genus

We describe three new species of forest robin in the genus Stiphrornis; two from West Africa and one from the Congo Basin. Each species represents a distinct phylogenetic lineage based on genetic analysis. In addition to genetic differentiation, each new species is diagnosable from other Stiphrornis lineages by morphology, and by plumage. One of the new species appears to be restricted to the Central and Brong-Ahafo Regions of Ghana, and another is restricted to Benin and the Central Region of Ghana. In Ghana, these two new species presumably come into contact with Stiphrornis erythrothorax (Western Region of Ghana and westward), and there is evidence that one of the new species has a distinguishably different song from erythrothorax. The distribution of the third new species is primarily on the south bank of the Congo River, near the city of Kisangani. Recognition of these species provides additional evidence that Afrotropical forests are harbouring substantial cryptic diversity, and that our knowledge of the drivers of this diversity remains poorly documented across the region.

http://www.zoobank.org/urn:lsid:zoobank.org:pub:BF2A0BE6-1140-4EFF-9035-380D61AB03AE     

The complex phylogeography of the Indo‐Malayan Alophoixus bulbuls with the description of a putative new ring species complex

The Indo‐Malayan bioregion has provided some of the most spectacular discoveries of new vertebrate species (e.g. saola, khanyou, bare‐faced bulbul) over the last 25 years. Yet, very little is known about the processes that led to the current biodiversity in this region. We reconstructed the phylogeographic history of a group of closely related passerines, the Alophoixus bulbuls. These birds are continuously distributed in Indo‐Malaya around the Thailand lowlands such that their distribution resembles a ring. Our analyses revealed a single colonization event of the mainland from Sundaland with sequential divergence of taxa from southwest to northeast characterized by significant gene flow between parapatric taxa, and reduced or ancient gene flow involving the two taxa at the extremities of the ring. We detected evidence of population expansion in two subspecies, including one that was involved in the closing of the ring. Hence, our analyses indicate that the diversification pattern of Alophoixus bulbuls fits a ring species model driven by geographic isolation. To our knowledge, the Alophoixus bulbuls represent the first case of a putative broken ring species complex in Indo‐Malaya. We also discuss the implications of our results on our understanding of the biogeography in Indo‐Malaya.     

Molecular markers and the species concept: New techniques to resolve old disputes?

Reviews in Fish Biology and Fisheries -     

When monophyly is not enough: exclusivity as the key to defining a phylogenetic species concept

A natural starting place for developing a phylogenetic species concept is to examine monophyletic groups of organisms. Proponents of “the” Phylogenetic Species Concept fall into one of two camps. The first camp denies that species even could be monophyletic and groups organisms using character traits. The second groups organisms using common ancestry and requires that species must be monophyletic. I argue that neither view is entirely correct. While monophyletic groups of organisms exist, they should not be equated with species. Instead, species must meet the more restrictive criterion of being genealogically exclusive groups where the members are more closely related to each other than to anything outside the group. I carefully spell out different versions of what this might mean and arrive at a working definition of exclusivity that forms groups that can function within phylogenetic theory. I conclude by arguing that while a phylogenetic species concept must use exclusivity as a grouping criterion, a variety of ranking criteria are consistent with the requirement that species can be placed on phylogenetic trees.

Systematics of the Saharo‐Arabian clade of the Palearctic naked‐toed geckos with the description of a new species of Tropiocolotes endemic to Oman

Geckos are one of the most species‐rich, abundant, and widely distributed of all Squamata lineages and present several characteristics that have made them favorite model organisms for biogeographical, ecological, physiological, and evolutionary studies. One of the key aspects of any comparative study is to have a robust, comprehensive phylogeny, and an updated taxonomy. Recently, the Infraorder Gekkota has been the subject of several phylogenetic analyses and taxonomic revisions at different levels. Despite all these phylogenetic and taxonomic advances, there are still some groups whose systematics and taxonomy remain highly problematic. Maybe one of the most poorly resolved groups in spite of decades of intensive research by many herpetologists are the so‐called Palearctic naked‐toed geckos of the family Gekkonidae. This group of nocturnal geckos distributed from Mauritania across North Africa, Arabia, southwestern and central Asia to northern India, western China and southern Mongolia is characterized by the synapomorphy of lack of adhesive subdigital pads. Within the Palearctic naked‐toed geckos, the Saharo‐Arabian clade comprised by the genera Pseudoceramodactylus, Stenodactylus, and Tropiocolotes is the clade with the largest distribution range. At the same time, it is one of the problematic groups, presenting poorly supported phylogenetic relationships, with the genus Tropiocolotes being recovered non‐monophyletic in all analyses despite its morphological uniformity. To reassess the phylogeny of the Palearctic naked‐toed geckos with a special interest in the systematics of Tropiocolotes, we assembled a dataset comprising 298 gecko specimens from 283 different species (including all Tropiocolotes species but one) belonging to 122 of a total of 124 described gecko genera. This dataset included the nuclear c‐mos, ACM4, RAG1, RAG2, and PDC and the mitochondrial ND2 gene. To further investigate the relationships within Tropiocolotes and to revise the systematics of the south Arabian endemic species Tropiocolotes scorteccii, we used an integrative approach including information from the nuclear MC1R and c‐mos, the mitochondrial 12S, 16S, cytb genes, and morphological data from nine of the 10 described Tropiocolotes species. The phylogenetic analyses of the Gekkota dataset recovered a similar topology for the Palearctic naked‐toed geckos to previous studies, but in this case, Tropiocolotes was recovered monophyletic in all analyses, with high support in two of them. The results of the analyses of three datasets specifically assembled to test the effect of both gene sampling and taxon sampling in the monophyly of Tropiocolotes, and the internal relationships of the Palearctic naked‐toed geckos clearly showed that both the number and kind of characters (nuclear or mitochondrial data) and the number of taxa played a fundamental role in recovering the correct phylogenetic relationships. The phylogenetic analyses within Tropiocolotes suggested the existence of high levels of undescribed diversity in the south Arabian T. scorteccii, including a new genetically and morphologically distinct species endemic to Oman (Tropiocolotes confusus sp. nov. ). Our study using a large dataset, including several loci and a dense taxon sampling within Gekkota and especially within Tropiocolotes, has proved a valuable strategy to address the monophyly of Tropiocolotes and the relationships within the Saharo‐Arabian Palearctic naked‐toed geckos. The integrative systematic approach including several samples of south Arabian T. scorteccii based on many years of fieldwork has, once more, uncovered a new species endemic to this region. This highlights the importance of this area of Arabia as a reservoir of reptile endemicity and biodiversity, which is likely linked to the high degree of habitat heterogeneity and the effect of the monsoons. Obviously, based on this and previously published evidence, south Arabia represents an area with still high levels of undiscovered diversity.     

Cryptic diversity in the Mexican highlands: Thousands of UCE loci help illuminate phylogenetic relationships,species limits and divergence times of montane rattlesnakes (Viperidae: Crotalus)

With the continued adoption of genome‐scale data in evolutionary biology comes the challenge of adequately harnessing the information to make accurate phylogenetic inferences. Coalescent‐based methods of species tree inference have become common, and concatenation has been shown in simulation to perform well, particularly when levels of incomplete lineage sorting are low. However, simulation conditions are often overly simplistic, leaving empiricists with uncertainty regarding analytical tools. We use a large ultraconserved element data set (>3,000 loci) from rattlesnakes of the Crotalus triseriatus group to delimit lineages and estimate species trees using concatenation and several coalescent‐based methods. Unpartitioned and partitioned maximum likelihood and Bayesian analysis of the concatenated matrix yield a topology identical to coalescent analysis of a subset of the data in bpp . ASTRAL analysis on a subset of the more variable loci also results in a tree consistent with concatenation and bpp , whereas the SVDquartets phylogeny differs at additional nodes. The size of the concatenated matrix has a strong effect on species tree inference using SVDquartets , warranting additional investigation on optimal data characteristics for this method. Species delimitation analyses suggest up to 16 unique lineages may be present within the C. triseriatus group, with divergences occurring during the Neogene and Quaternary. Network analyses suggest hybridization within the group is relatively rare. Altogether, our results reaffirm the Mexican highlands as a biodiversity hotspot and suggest that coalescent‐based species tree inference on data subsets can provide a strongly supported species tree consistent with concatenation of all loci with a large amount of missing data.     

Cryptic species as a window into the paradigm shift of the species concept

The species concept is the cornerstone of biodiversity science, and any paradigm shift in the delimitation of species affects many research fields. Many biologists now are embracing a new “species” paradigm as separately evolving populations using different delimitation criteria. Individual criteria can emerge during different periods of speciation; some may never evolve. As such, a paradigm shift in the species concept relates to this inherent heterogeneity in the speciation process and species category—which is fundamentally overlooked in biodiversity research. Cryptic species fall within this paradigm shift: they are continuously being reported from diverse animal phyla but are poorly considered in current tests of ecological and evolutionary theory. The aim of this review is to integrate cryptic species in biodiversity science. In the first section, we address that the absence of morphological diversification is an evolutionary phenomenon, a “process” counterpart to the long‐studied mechanisms of morphological diversification. In the next section regarding taxonomy, we show that molecular delimitation of cryptic species is heavily biased towards distance‐based methods. We also stress the importance of formally naming of cryptic species for better integration into research fields that use species as units of analysis. Finally, we show that incorporating cryptic species leads to novel insights regarding biodiversity patterns and processes, including large‐scale biodiversity assessments, geographic variation in species distribution and species coexistence. It is time for incorporating multicriteria species approaches aiming to understand speciation across space and taxa, thus allowing integration into biodiversity conservation while accommodating for species uncertainty.     

Integrative taxonomy of Flatbill Flycatchers (Tyrannidae) reveals a new species from the Amazonian lowlands

Integrative taxonomic studies continue to reveal that many current polytypic species of birds are in fact constituted by two or more species and therefore have been central in uncovering ‘hidden’ or ‘cryptic’ biodiversity. The Olivaceous Flatbill (Aves: Tyrannidae: Rhynchocyclus olivaceus) currently has nine recognized subspecies distributed throughout the Neotropics, but so far, no complete phylogenetic hypothesis exists to test the validity and evolutionary relationships among them. To remedy this, we conducted a multi-character integrative taxonomic revision of the genus Rhynchocyclus, focusing on the polytypic R. olivaceus. The combination of a taxonomically dense sampled multilocus phylogeny (including three mitochondrial and two nuclear genes) with phenotypic analyses including morphological and vocal characters pointed to several taxonomic inconsistencies within R. olivaceus. The analyses strongly support that R. olivaceus is paraphyletic, with an exclusively cis-Andean clade (where the topotypic R. olivaceus is found) clustering as sister to Rhynchocyclus fulvipectus, to the exclusion of a clade grouping trans-Andean and western Amazonian populations currently placed in R. olivaceus—one of which is unnamed and fully diagnosable based on vocal and genetic characters. Consistent with the phylogenetic results, our vocal analyses identified at least four morphologically cryptic lineages within R. olivaceus that can be mutually diagnosed from each other by different loudsongs and call parameters. Therefore, we provide evidence for splitting these four groups into separate species, two of which are sympatric but not syntopic in western Amazonia, including an unnamed species described herein—Rhynchocyclus cryptus, sp. nov. urn:lsid:zoobank.org:act:2DC17190-2BDD-49EC-88E6-4CF2FC2562A3.     

Allozymic variation and divergence in three species of Antirrhinum L. (Scrophulariaceae-Antirrhineae)

An allozymic study of three wild species of Antirrhinum L. A. lopesiamum Rothm., A. mollissimum Roihni. and A. microphyllum Rothm. is described. All are members of subsection Kickiella Rothm., and are narrow-range endemics of the Iberian Peninsula. The variability of the different loci, as well as the number and mobility of the alleles, differ among the three species, a demonstration of the usefulness of allozymes for the systematics of the genus. The finding of alleles unique to each species indicates high divergence among species suggesting ancient diversification, and supports the hypothesis of a geographical model of speciation. All three species show high levels of within-species variability, mainly partitioned within populations, while between populations genetic differentiation is low. Correlations between population size, sample size and genetic variability, and the usefulness of allozymic data for conservation purposes, are discussed.     

Taxonomy of Selaginella: a study of characters, techniques, and classification in the Hong Kong species

This study of 11 Hung Kong species of Selaginella indicates that sufficient characters exist by which they may be conveniently, consistently, and conclusively distinguished, and implies that the same is true for the rest of the genus, which suffers from chronic taxonomic confusion. Characters assessed are: leaf size, shape, epidermal cell patterns and mesophyll structure; ligule shape; patterns seen in stem transections; sporophyll shape; microsporangium shape; sporangial distribution; and spore surface ornamentation. Of these, the shape of median leaves, the maximum size of lateral leaves and epidermal cell patterns are the most significant and distinctive foliar features. These, together with spore surface ornamentation, are the most useful for distinguishing species. Correlations between the shapes of ligules, sporophylls, microsporangia, and vascular bundles indicate natural subgeneric groups.
These studies suggest that there are two ways by which taxonomic investigations of Selaginella can be improved. First leaves and spores should be prepared in permanent mountant (e.g. Hoyer's solution) for accurate observation of size, shape, and epidermal patterns. Secondly, data should be collected on a wide range of features.     

基于生物学物种定义探讨物种形成理论与验证的研究进展

物种形成是进化生物学研究的一个永恒主题, 由于生物群体进化是连续和动态的, 物种界限变得难于界定。本文首先讨论了3种地理物种形成模式(同域、邻域及异域), 并分析了近期报道的研究证据。其次, 评述了合子后生殖隔离机制的分子遗传基础和应用群体基因组数据分析的证据, 包括BDMI模型(Bateson-Dobzhansky-Muller incompatibility)、QTLs (quantitative trait loci)、霍尔丹法则及大X染色体效应。最后, 探讨了交配系统作为合子前隔离机制之一与物种形成的关系, 认为近交或自交通过扩大种群遗传结构分化, 增强不同交配系统的种群间不对称基因渐渗, 或种群间无基因渐渗等途径, 促进新物种形成。已知植物交配系统的演化更倾向于从异交(或自交不亲和)向自交(或近交亲和)方式, 花性状和基因组的分化推动形成所谓的自交综合征, 研究交配系统驱动或强化物种形成模式对认识植物物种形成机制有重要意义。     

Morphological differentiation among closely related species with disjunct distributions: a case study of Mediterranean Cyclamen L. subgen. Psilanthum Schwarz (Primulaceae)

In Cyclamen subgenus Psilanthum , previous authors have recognized three species ( C. repandum, C. balearicum and C. creticum ), with C. repandum subdivided into three subspecies (ssp. repandum , ssp. peloponnesiacum and ssp. rhodense ), and two varieties (var. vividum and var. peloponnesiacum ) within C. repandum ssp. peloponnesiacum . To examine the validity of this classification and the degree of morphological differentiation among closely related endemic taxa with disjunct distributions, we undertook analyses of three quantitative and eight qualitative morphological traits of flowers and leaves, most of which have previously been used without statistical comparison in the classification of the different taxa. Cyclamen balearicum showed high levels of morphological differentiation from all other taxa in subgenus Psilanthum consistent with its specific status. In contrast, morphological differentiation between C. creticum and subspecies of C. repandum was similar to that among the three subspecies of C. repandum . When compared with a recent molecular phylogeny of this subgenus, our results suggest that C. creticum may best be described as a geographical subspecies of C. repandum . The two varieties of C. repandum ssp. peloponnesiacum showed few significant differences for individual traits and their overall morphology is very similar to each other. The morphology of plants at three sites on Corsica strongly suggest, consistent with molecular data, the occurrence of hybrid populations between C. balearicum (outside of its previously recognized distribution) and local C. repandum .  © 2002 The Linnean Society of London, Botanical Journal of the Linnean Society , 2002, 139 , 133–144.     

Evidence for parallel ecological speciation in scincid lizards of the Eumeces skiltonianus species group (Squamata: Scincidae)

We identify instances of parallel morphological evolution in North American scincid lizards of the Eumeces skiltonianus species group and provide evidence that this system is consistent with a model of ecological speciation. The group consists of three putative species divided among two morphotypes, the small-bodied and striped E. skiltonianus and E. lagunensis versus the large-bodied and typically uniform-colored E. gilberti. Members of the group pass through markedly similar phenotypic stages during early development, but differ with respect to where terminal morphology occurs along the developmental sequence. The morphotypes also differ in habitat preference, with the large-bodied gilberti form generally inhabiting lower elevations and drier environments than the smaller, striped morphs. We inferred the phylogenetic relationships of 53 skiltonianus group populations using mtDNA sequence data from the ND4 protein-coding gene and three flanking tRNAs (900 bp total). Sampling encompassed nearly the entire geographic range of the group, and all currently recognized species and subspecies were included. Our results provide strong evidence for parallel origins of three clades characterized by the gilberti morphotype, two of which are nested within the more geographically widespread E. skiltonianus. Eumeces lagunensis was also nested among populations of E. skiltonianus. Comparative analyses using independent contrasts show that evolutionary changes in body size are correlated with differences in adult color pattern. The independently derived association of gilberti morphology with warm, arid environments suggests that phenotypic divergence is the result of adaptation to contrasting selection regimes. We provide evidence that body size was likely the target of natural selection, and that divergences in color pattern and mate recognition are probable secondary consequences of evolving large body size.     

The species concept as an emergent property of population biology

Resurgent interest in the genetics of population divergence and speciation coincides with recent critical evaluation of species concepts and proposals for species delimitation. An important result of these parallel trends is a slight but important conceptual shift in focus away from species diagnoses based on prior species concepts or definitions, and toward analyses of the processes acting on lineages of metapopulations that eventually lead to differences recognizable as species taxa. An advantage of this approach is that it identifies quantitative metapopulation differences in continuous variables, rather than discrete entities that do or do not conform to a prior species concept, and species taxa are recognized as an emergent property of population-level processes. The tension between species concepts and diagnosis versus emergent recognition of species taxa is at least as old as Darwin, and is unlikely to be resolved soon in favor of either view, because the products of both approaches (discrete utilitarian taxon names for species, process-based understanding of the origins of differentiated metapopulations) continue to have important applications.