Lack of reproductive isolation between the Western and Eastern phylogroups of the tench

The Eurasian range of the tench distribution is subdivided into deeply divergent Western and Eastern phylogroups evidenced by nuclear and mitochondrial DNA sequence markers. A broad zone of overlap exists in central and western Europe, suggesting post-glacial contact with limited hybridisation. We conducted a population genetic test of this indication that the two phylogroups may represent distinct species. We analysed variation at introns of nuclear genes, microsatellites, allozymes and mitochondrial DNA in populations from two postglacial lakes within the contact zone in Germany. The test is based on the expectation that in the presence of strong barriers to reproduction, a hybrid population will show genome-wide associations among alleles and genotypes from each phylogroup even after hundreds of generations of interbreeding. In contrast to this expectation, no consistent significant deviations from linkage and Hardy–Weinberg equilibria were found. Samples from both lakes did show significant disequilibria but they were limited to individual loci and were not concordant between populations, and were not robust to the method used. The single consistent association can be attributed to physical linkage between two microsatellite loci. Thus, results of our study support the hypothesis of free interbreeding between the two phylogroups of tench. Therefore, although the phylogroups may be considered as separate phylogenetic species, the present data suggest that they are a single species under the biological species concept.     

PHYLOGENETIC SYSTEMATICS AND THE SPECIES PROBLEM

Abstract— A tension has arisen over the primacy of interbreeding versus monophyly in defining the species category. Manifestations of this tension include unnecessary restriction of the concept of monophyly as well as inappropriate attribution of "species" properties, to "higher taxa", and vice versa. Distinctions between systems (wholes) deriving their existence from different underlying. processes have been obscured by failure to acknowledge different interpretations of the concept of individuality. We identify interbreeding (resulting in populations) and evolutionary descent (resulting in monophyletic groups) as two processes of interest to phylogenetic systematists, and explore the relations between the systems resulting from these processes. In the case of sexual reproduction, populations of interbreeding organisms (regardless of whether they are monophyletic) exist as cohesive wholes and play a special role in phylogenetic systematics, being the least inclusive entities appropriate for use as terminal units in phylogenetic analysis of organismal relationships. Both sexual and asexual organisms form monophyletic groups. Accepting the reality and significance of both interbreeding and monophyly emphasizes that a conscious decision must be made regarding which phenomenon should be used to define the species category. Examination of species concepts that focus either on interbreeding or on common descent leads us to conclude that several alternatives are acceptable from the standpoint of phylogenetic systematics but that no one species concept can meet the needs of all comparative biologists.     

Pre‐ and post‐mating reproductive barriers drive divergence of five sympatric species of Naryciinae moths (Lepidoptera: Psychidae)

The biological species concept suggests that species can be separated on the basis of reproductive isolation. However, because natural interbreeding capabilities are often unknown, differences in morphology are generally used to separate species. Alternatively, genetic dissimilarity is used to separate morphologically similar species. Many genetic markers, including the maternally inherited mitochondrial cytochrome oxidase I sequence, cannot show interbreeding and therefore species status of groups may remain unresolved. In species of the genera Dahlica and Siederia (Lepidoptera: Psychidae: Naryciinae) the lack of morphological distinction and unknown interbreeding has led to unclear and unresolved taxonomic status. Mitochondrial DNA sequences suggest five sexual species to occur in Finland. However, their species status remains unconfirmed, due to a lack of knowledge on interbreeding, unclear morphological distinction and the limited variation in mitochondrial DNA. We combine three methods, a cross‐mating experiment, an analysis of mitochondrial and nuclear DNA, and a detailed male genital morphological examination, to establish the species status of the five suspected species. All suspected species exhibit intraspecies mating preference, although several interspecies pairs readily produce offspring. The genetic analysis, however, fails to show hybrids or introgression, suggesting that both pre‐ and post‐copulation mechanisms isolate the species reproductively. Morphological analysis of the male genitalia confirms that the species have diverged. Our results highlight the need of combining behavioural, morphological and genetic methods to determine species status in challenging taxonomic groups. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112 , 584–605.     

Species concepts and species reality: salvaging a Linnaean rank

The validity of the species category (rank) as a distinct level of biological organization has been questioned. Phenetic, cohesion and monophyletic species concepts do not delimit species-level taxa that are qualitatively distinct from lower or higher taxa: all organisms throughout the tree of life exhibit varying degrees of similarity, cohesion, and monophyly. In contrast, interbreeding concepts delimit species-level taxa characterized by a phenomenon (regular gene flow) not found in higher taxa, making the species category a distinct level of biological organization. Only interbreeding concepts delimit species-level taxa that are all comparable according to a biologically meaningful criterion and qualitatively distinct from entities assigned to other taxonomic categories. Consistent application of interbreeding concepts can result in counterintuitive taxonomies--e.g. many wide polytypic species in plants and narrow cryptic species in animals. However, far from being problematic, such differences are biologically illuminating--reflecting differing barriers to gene flow in different clades. Empirical problems with interbreeding concepts exist, but many of these also apply to other species concepts, whereas others are not as severe as some have argued. A monistic view of species using interbreeding concepts will encounter strong historical inertia, but can save the species category from redundancy with other categories, and thus justify continued recognition of the species category.     

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.     

Two in one: cryptic species discovered in biological control agent populations using molecular data and crossbreeding experiments

There are many examples of cryptic species that have been identified through DNA‐barcoding or other genetic techniques. There are, however, very few confirmations of cryptic species being reproductively isolated. This study presents one of the few cases of cryptic species that has been confirmed to be reproductively isolated and therefore true species according to the biological species concept. The cryptic species are of special interest because they were discovered within biological control agent populations. Two geographically isolated populations of Eccritotarsus catarinensis (Carvalho) [Hemiptera: Miridae], a biological control agent for the invasive aquatic macrophyte, water hyacinth, Eichhornia crassipes (Mart.) Solms [Pontederiaceae], in South Africa, were sampled from the native range of the species in South America. Morphological characteristics indicated that both populations were the same species according to the current taxonomy, but subsequent DNA analysis and breeding experiments revealed that the two populations are reproductively isolated. Crossbreeding experiments resulted in very few hybrid offspring when individuals were forced to interbreed with individuals of the other population, and no hybrid offspring were recorded when a choice of mate from either population was offered. The data indicate that the two populations are cryptic species that are reproductively incompatible. Subtle but reliable diagnostic characteristics were then identified to distinguish between the two species which would have been considered intraspecific variation without the data from the genetics and interbreeding experiments. These findings suggest that all consignments of biological control agents from allopatric populations should be screened for cryptic species using genetic techniques and that the importation of multiple consignments of the same species for biological control should be conducted with caution.     

Individuality,pluralism, and the phylogenetic species concept

The concept of individuality as applied to species, an important advance in the philosophy of evolutionary biology, is nevertheless in need of refinement. Four important subparts of this concept must be recognized: spatial boundaries, temporal boundaries, integration, and cohesion. Not all species necessarily meet all of these. Two very different types of pluralism have been advocated with respect to species, only one of which is satisfactory. An often unrecognized distinction between grouping and ranking components of any species concept is necessary. A phylogenetic species concept is advocated that uses a (monistic) grouping criterion of monophyly in a cladistic sense, and a (pluralistic) ranking criterion based on those causal processes that are most important in producing and maintaining lineages in a particular case. Such causal processes can include actual interbreeding, selective constraints, and developmental canalization. The widespread use of the biological species concept is flawed for two reasons: because of a failure to distinguish grouping from ranking criteria and because of an unwarranted emphasis on the importance of interbreeding as a universal causal factor controlling evolutionary diversification. The potential to interbreed is not in itself a process; it is instead a result of a diversity of processes which result in shared selective environments and common developmental programs. These types of processes act in both sexual and asexual organisms, thus the phylogenetic species concept can reflect an underlying unity that the biological species concept can not.     

Regarding the confusion between the population concept and Mayr's "population thinking"

Ernst Mayr said that one of Darwin's greatest contributions was to show scholars the way to population thinking, and to help them discard a mindset of typological thinking. Population thinking rejects a focus on a central representative type, and emphasizes the variation among individuals. However, Mayr's choice of terms has led to confusion, particularly among biologists who study natural populations. Both population thinking and the concept of a biological population were inspired by Darwin, and from Darwin the chain for both concepts runs through Francis Galton who introduced the statistical usage of "population" that appears in Mayr's population thinking. It was Galton's "population" that was modified by geneticists and biometricians in the early 20th century to refer to an interbreeding and evolving community of organisms. Under this meaning, a population is a biological entity and so paradoxically population thinking, which emphasizes variation at the expense of dwelling on entities, is usually not about populations. Mayr did not address the potential for misunderstanding but for him the important part of the population concept was that the organisms within a population were variable, and so he probably thought there should not be confusion between population thinking and the concept of a population.     

Speciation in the fossil record

It is easy to claim that the fossil record says nothing about speciation because the biological species concept (which relies on interbreeding) cannot be applied to it and genetic studies cannot be carried out on it. However, fossilized organisms are often preserved in sufficient abundance for populations of intergrading morphs to be recognized, which, by analogy with modern populations, are probably biological species. Moreover, the fossil record is our only reliable documentation of the sequence of past events over long time intervals: the processes of speciation are generally too slow to be observed directly, and permanent reproductive isolation can only be verified with hindsight. Recent work has shown that some parts of the fossil record are astonishingly complete and well documented, and patterns of lineage splitting can be examined in detail. Marine plankton appear to show gradual speciation, with subsequent morphological differentiation of lineages taking up to 500000 years to occur. Marine invertebrates and vertebrates more commonly show punctuated patterns, with periods of rapid speciation followed by long-term stasis of species lineages.     

When the Rule Becomes the Exception. No Evidence of Gene Flow between Two Zerynthia Cryptic Butterflies Suggests the Emergence of a New Model Group

There is increasing evidence that most parapatric cryptic/sister taxa are reproductively compatible across their areas of contact. Consequently, the biological species concept, which assumes absence of interbreeding, is becoming a not so effective criterion in evolutionary ecology. Nevertheless, the few parapatric sister taxa showing complete reproductive barriers represent interesting models to study speciation processes and the evolution of reproductive isolation. In this study, we examined contact populations in northwestern Italy of two butterfly species, Zerynthia polyxena and Z. cassandra, characterized by different genitalic morphotypes. We studied levels of divergence among 21 populations distributed from Sicily to France using three genetic markers (the mitochondrial COI and ND1 genes and the nuclear wingless gene) and genitalic geometric morphometrics. Moreover, we performed species distribution modelling to estimate different climatic requirements of Z. polyxena and Z. cassandra. We projected climatic data into glacial maximum scenarios in order to verify if and to which extent glacial cycles could have contributed to speciation processes. Genetic and morphometric analyses identified two main groups. All specimens showed a concordant pattern of diversification, including those individuals sampled in the contact area. Haplotype distribution and climatic models showed that during glacial maxima both species experienced a strong range contraction and presumably remained separated into different microrefugia in southern France, in the Italian Peninsula and on the islands of Elba and Sicily. Long term separation was probably favoured by reduced dispersal ability and high phylopatry, while genitalic diversification probably favoured interbreeding avoidance. Conversely, the aposematic wing pattern remained almost identical. We compared our results with those obtained in other species and concluded that Z. polyxena and Z. cassandra represent a valuable model in the study of speciation.     

Modern humans did not admix with Neanderthals during their range expansion into Europe

The process by which the Neanderthals were replaced by modern humans between 42,000 and 30,000 before present is still intriguing. Although no Neanderthal mitochondrial DNA (mtDNA) lineage is found to date among several thousands of Europeans and in seven early modern Europeans, interbreeding rates as high as 25% could not be excluded between the two subspecies. In this study, we introduce a realistic model of the range expansion of early modern humans into Europe, and of their competition and potential admixture with local Neanderthals. Under this scenario, which explicitly models the dynamics of Neanderthals' replacement, we estimate that maximum interbreeding rates between the two populations should have been smaller than 0.1%. We indeed show that the absence of Neanderthal mtDNA sequences in Europe is compatible with at most 120 admixture events between the two populations despite a likely cohabitation time of more than 12,000 y. This extremely low number strongly suggests an almost complete sterility between Neanderthal females and modern human males, implying that the two populations were probably distinct biological species.     

The cladistic solution to the species problem

The correct explanation of why species, in evolutionary theory, are individuals and not classes is the cladistic species concept. The cladistic species concept defines species as the group of organisms between two speciation events, or between one speciation event and one extinction event, or (for living species) that are descended from a speciation event. It is a theoretical concept, and therefore has the virtue of distinguishing clearly the theoretical nature of species from the practical criteria by which species may be recognized at any one time. Ecological or biological (reproductive) criteria may help in the practical recognition of species. Ecological and biological species concepts are also needed to explain why cladistic species exist as distinct lineages, and to explain what exactly takes place during a speciation event. The ecological and biological species concepts work only as sub-theories of the cladistic species concept and if taken by themselves independently of cladism they are liable to blunder. The biological species concept neither provides a better explanation of species indivudualism than the ecological species concept, nor, taken by itself, can the biological species concept even be reconciled with species individualism. Taking the individuality of species seriously requires subordinating the biological, to the cladistic, species concept.     

The debate about the biological species concept - a review

The importance of the species concept in biology has led to a continuing debate about the definition of species. This paper summarizes the recent literature in relation to the ‘biological species concept’ (MAYR 1942). Among the general attributes demanded, possible limitations of the universality and applicability of a species definition are discussed. Three different areas of criticism of the biological species concept are considered: 1. The impracticability of the criterion of reproductive isolation. The demand for more practical criteria is rejected, because reproductive isolation is seen as the factor that produces and maintains species as discrete entities in nature. 2. The inapplicability to non-bisexual organisms. A brief survey of modes of uniparental reproduction and their relative importance suggests that obligatory apomicts are of little evolutionary significance. 3. The inapplicability to multidimensional situations. Despite practical difficulties, the biological species concept is held to apply to organisms separated in space. The impossibility to delimit species in time by reproductive isolation is recognized. Out of two ways to divide continuous evolutionary lineages in time, the phylogenetic approach, which considers only speciation events (cladogenesis), is preferred as it is more objective. A list of recently published alternative definitions of species, none of which is found acceptable, is given. It is concluded that the biological species concept needs not be changed or dismissed on the basis of the discussed criticisms.     

Nuclear DNA polymorphisms in a wild population of yellow baboons (Papio hamadryas cynocephalus) from Mikumi National Park,Tanzania

Yellow baboons (Papio hamadryas cynocephalus) from Mikumi National Park, Tanzania were studied for polymorphisms in nuclear DNA. The study population consists of four social groups that inhabit overlapping home ranges and exchange males. As a result, these groups are considered to be members of a single interbreeding population. Human DNA clones were used as probes to screen five loci (AT3, REN, HEXB, VIM, and APOB) for restriction fragment length polymorphisms (RFLP). A total of 14 polymorphisms, at least one at each locus, was detected in a panel of 27 baboons tested using six restriction enzymes for each locus. Eleven of these RFLP systems have average heterozygosity values greater than 0.40. This initial screening demonstrates that human DNA clones can be used to detect significant numbers of informative DNA polymorphisms in single-copy nuclear genes of this species and suggests that the average proportion of nucleotides polymorphic across nuclear loci in this population may be between 1.0% and 1.3%. © 1993 Wiley-Liss, Inc.     

The end of Invasion Biology: intellectual debate does not equate to nonsensical science

Valéry et al. recently proposed to end the field of Invasion Biology on the grounds that it is based on an inadequate definition of the concept of biological invasion and that, as exotic species, native species should also be called invasive whenever they outbreak. We argue, on the contrary, that the sudden demographic dominance of native species cannot be termed invasion. Moreover, we claim that the suggestion of ending a fruitful and useful discipline because it does not conform to a subjective definition or because it still encompasses some debatable ideas and unresolved questions is both irrelevant and excessive. We believe that the thousands of researchers working in this discipline do not perform nonsensical science, and that their efforts to understand and limit biological invasions are compatible with debating on the key concept of that field.     

Experimental taxonomy of Australian mites in theMacrocheles glaber group (Acarina: Macrochelidae)

Mites which are abundant in southeastern Australia, and which have been tentatively identified asMacrocheles glaber on the basis of the appearance of the adult female, are shown to be a composite of two species when morphological features of the adult males are considered. These species are tentatively identified on morphological grounds asM. glaber (Müller) andM. perglaber Filipponi and Pegazzano. Populations of these two species imported from France are shown to be capable of interbreeding with their Australian counterparts, thus supporting the identification of the two species found in Australia.M. peregrinus Krantz, introduced into Australia from southern Africa, is shown to be incapable of interbreeding withM. perglaber. The demonstration thatM. glaber andM. perglaber both already exist in the field in Australia indicates that their deliberate introduction now would not contribute to the biological control of dung-breeding flies.     

Evolution,actuality and species concept: a need for a palaeontological tool

Species concept was developed to fit neontological necessities in ordering biological variability. Transversal (horizontal, synchronic) taxonomy shows hierarchical requirements quite different from those involved in longitudinal (vertical, diachronic) classifications. Furthermore, limitations within the species concept itself make it scarcely available in many paleontological contexts. Classical species definitions are often limited by theoretic and logic constraints, that are seldom available to describe practical situations. Morphology is an uncertain source of phylogenetic information, but it is still the main ground of biological comparison for extinct populations. Therefore, efforts in species recognition should be devoted to making taxonomy a useful tool for communication. First, inferences in systematics have to be led upon the available information about characters and processes. If this information is missing or not developed, no detailed conclusions can be supported. Secondly, definitions should be sufficiently elastic and generalised to allow an adaptation to each different case-study. The final target is to synthesise actual evolutionary histories, and not biological potentialities.     

What is a fish species?

The formal processes of alpha-taxonomy ensure that species have uniquenames and can be identified. No similar process is mandatory forinfraspecific variation, so the species is a uniquely importantpractical term. At present, there is little agreement of the definitionof a species. In the last 30 years, numerous concepts have beenproposed. The nature of fish species is reviewed. Clonal inheritance ofnuclear genes occurs in several lineages. Hybridization is frequent,often leading to introgression, which may lead to extinction of species.Species may have hybrid origins. There is good evidence for parallelspeciation in similar habitats. There are clearly exceptions to thecladistic assumption of dichotomous branching during speciation. Siblingspecies may exist with no discernible niche differentiation.Basic assumptions are violated for the recognition, phylogenetic,ecological and some formulations of the evolutionary species concepts.The most satisfactory definitions are two of the earliest proposed inthe light of evolutionary theory. The Darwinian view is that species arerecognizable entities which are not qualitatively distinct fromvarieties. A restatement of this concept in genetic terms provides ameans of dealing with all forms of species known in present-day fishes.This modified Darwinian concept is operated through the application offuzzy logic rather than rigid definition. This involves a search fordiscontinuities between species, rather than an a priori definition ofhow boundaries are to be determined. A subset of Darwinian species areMayrian or biological species, which are characterized by theirdemonstrable reproductive isolation from other species. The status of apopulation as a Mayrian species is a testable hypothesis. Moleculartechniques allow this hypothesis to be tested more easily thanpreviously, at least when dealing with sympatric populations.     

Two fish species competition model with nonlinear interactions and equilibrium catches

Two species competition model is built up by assuming the hypothetical second order interactions in order to consider effects of exploitation on two competing fish species with non-linear interactions. Most important characteristic of this model, compared withLotka-Volterra type linear competition model, is that this model can possess multiple stable equilibrium points. Therefore there is a possibility that two species keeping the equilibrium state at one stable equilibrium point will be attracted to the other stable equilibrium point after a heavy perturbation. In this model reversible change of the fishing pressure does not always results in that of the equilibrium catch. In this sence MSY concept for single species can not be extended to this model. If there are multiple stable equilibrium points, the change of the dominant fish species, catastrophic and irreversible change of each equilibrium catch may be observed when the perturbation by the exploitation is added. This phenomenon immediately reminds us of the change of the dominant fish species between Japanese common mackerel and Pacific saury in the northwest Pacific Ocean. In case of the management of two competing fish species with nonlinear interactions, the consideration on the balance between the fishing pressure for each species may be as important as the decision on the catch limit for each species. MSY level for each species based on the single-species theory could be quite erroneous.