A pragmatic approach to the species problem from a paleontological perspective

Given these remarkable developments, and the three decades that have elapsed since the last comprehensive-and magisterial-treatments of plant speciation and evolution by Levin was a hero of my youth, who had made his name in plant population biology, but also added substantially to our understanding of speciation through his research on the genus Phlox (Polemoniaceae). His contributions included early studies of plant demography, genetic differentiation among populations, divergence in pollination biology among closely related species, selection for reproductive isolation, and constraints on species ranges.

Speciation genetics explores the genetic mechanisms and processes underlying the formation of new species, focusing on how reproductive isolation and divergence arise through genetic changes. The term speciation was coined by Cook in 1906. Basically speciation involves two processes: Anagenesis and cladogenesis (true speciation). Anagenesis means phyletic change in the course of geological time or the transformation of old species into a new one in due course of time i.e. transformation in time. Cladogenesis or true speciation means origin of new species of organisms through splitting of the pre-existing ones. During the phyletic change in the process of anagenesis, there is no role of reproductive isolation because one species is transformed into another one. However, during cladogenesis, one species splits into two or more populations, they gradually accumulate genetic changes through the action of mutation, recombination, selection, genetic drift and migration and when they become geographically isolated, develop reproductive isolating mechanisms and acquire the status of new species. The origin and development of reproductive isolating mechanism are considered as pre requisite for the process of speciation. It has been rightly remarked that based on Biological Species Concept, the question should be asked how reproductive isolating mechanisms are established instead of asking how new species evolve. In the process of speciation, three components are involved: mechanisms generating genetic variability, origin of reproductive isolating mechanisms and geographic component (ranging from allopatry to sympatry). Species is a Latin word which means kind. Species is a basic unit as well as considered as basic category of biological classification which has been defined in different manner under different concepts of species. Initially the first species concept was morphological/typological/essentialist species concept which was explained by Linnaeus in eighteenth century but it was finally discarded because of morphological variations within the species and the occurrence of sibling species which are morphologically similar but reproductively isolated. Later, in seventeenth and eighteenth century, there was emergence of idea of reproductive relationship by Ray and Koelreuter which paved the way for Biological species concept. Darwin also gave importance to biological species concept because he also believed in the role of reproductive isolation in speciation. In twentieth century, the biological species concept was elaborated and developed in detail by Jordan, Mayr and Dobzhansky. Under this species concept, the species is defined as a group of potentially or actually interbreeding individuals which are reproductively isolated from other such groups. However, it has certain difficulties in its application. de Queiroz argues that there is single, primary species concept that is adequate –applying across biodiversity and that is the general lineage concept. Recently, a new species concept, genic species concept has been proposed by a molecular evolutionary biologist Wu who severely criticized biological species concept and suggested that it should be abandoned. According to genic species concept, it is not the whole genome, but a gene is unit of speciation. Thus speciation genes are responsible for creation of new species or cladogenesis. In Drosophila, hybrid male sterility has been frequently studied and the genes involved are known to play role in speciation. It has also been argued that there are two models, with the respect of number of loci involved in hybrid sterility. The first model states that there are a number of segregating units (polygenes) involved in hybrid sterility each with small effect. In the second architecture, it is suggested that there are one or a few genes of large effect involved in hybrid sterility leading to speciation. In this review, while taking the examples of hybrid sterility from Drosophila, an excellent biological model, speciation genetics as an emerging area of evolutionary biology is discussed keeping in view the biological species concept as well as genic species concept of species.

What is a species? This is a question seemingly simple but difficult to be addressed clearly. If only by a simple definition, a “species” can be described as the basic category or unit for taxonomic classification of organisms (including animals, plants, and microbes). On the other hand, it is extremely difficult to define a “species” or “species concept” that are generally acceptable by all biologists. Substantial debates exist over the “species concept” and have lasted for more than a contrary. During this time span, many species concepts have been proposed by various groups of biologists who work in different disciplines. However, it is extremely difficult to have a clear definition for “species” and particularly for “species concept” that are universally agreeable. Among the proposed species concepts, only some of them are influential, including those: taxonomic species concept, Darwin’s species concept, biological species concept, genetic species concept, and phylogenetic species concept. Obviously, biologists who proposed their species concepts attempt to interpret what “species” are only by emphasizing the specific features of a species appreciable from their perspectives. For example, biologists who have proposed taxonomic species concept highlight the classification feature of a species; whereas those who have Darwin’s species concept stress the evolutionary process of a species. Disagreements always exist among biologists when define the species concept. Some biologists believe that a species is a natural unit, which is strictly followed for the classification of a species. However, other biologists do not believe a species to be a natural unit, instead, they emphasize more on the evolution and reproductive aspects of a species. The extreme groups even reject “species” as a natural units. They only accept individuals as the natural unit. Obviously, the dilemma is due to the diverged understanding and opinion of species. We know that species are the outcomes of evolution—biodiversity. From the practical viewpoint, it is necessary to categorize the evolution-resulted biodiversity using a stable classification system. Therefore, taxonomists prefer to use a discontinued unit to classify species. On the other hand, evolutionists emphasize more on the variation of organisms. Thus, the characteristics of evolutionary continuity and taxonomic discontinuity have stimulated such debates over a species—a natural unit or an artificial category. Species are outcomes of continued evolutionary process and categories of discontinued taxonomy. As such, one can recognize, understand, and define a species according to the objectives and demands to suit his or her research, without being troubled too much by a universally unified concept of species. Thus, to answer what is a species, we prefer the definition that a species is an individual collection that occurs in a particularly space/time, shares similar morphological and physiological features with a common ancestor. Members of the same species are able to interbreed and reproduce normal descendants.

The term species is a Latin word meaning kinds. Species is a basic unit of biological classification as well as taxonomic rank. The scientific system of giving names to kinds of plants and animals revolves around the level of species. Early Greek philosophers such as Hippocrates, Plato and Aristotle also emphasized on the biological classification. Aristotle was considered as father of biological classification and he emphasized that all the parts of the body and activity should be considered during classification. As far as species is considered his idea was basically of essentialism or typological. Later on, in eighteenth century, the typological species concept also called as essentialism was elaborated by Linnaeus who was considered as father of taxonomy and proposed binomial nomenclature. In eighteenth century, a new concept of species called as Nominalistic species concept was suggested by Occam and his followers which was very popular in France. It states that nature produces individuals and nothing else. Species has no real existence in nature and it is only a mental concept. In seventeenth century, a new species concept began to emerge and it was Ray who believed in morphological species concept, but his species characteristics also contained the germ of biological species concept because he considered the reproductive relationship to be a principal species criterion. As early as 1760, Koelreutier also emphasized that all the individuals which are able to interbreed and produce fertile offspring belong to the same species. Other naturalists and taxonomists of nineteenth century such as Buffon, Merrem, Voigt, Walsh, and many others prepared the way for development of biological species concept. Charles Darwin who proposed the theory of origin of species by means of natural selection, appeared to have a morphological concept of species which was central to his theory of natural selection. However, later he gave importance to reproductive isolation and hence biological species concept. In his transmutation notebooks, Darwin realized the reality of species on the basis of criterion of non-interbreeding. As a consequence of this, biological species concept, Darwin recognized that acquisition of reproductive isolation was the mark of completion of transformation of permanent variety to the status of good species. Later on, biological species concept was emphasized and developed by Jordan, Mayr and Dobzhansky in the twentieth century. However, it has certain difficulties in its applications. According to this species concept, species is defined as a group of potentially or actually interbreeding natural populations which are reproductively isolated from other such groups. It was accepted as a most widely accepted definition of species. However, recently it has been criticized by molecular evolutionary biologists stating that “It is the time to abandon the biological species concept”. At the same time, it is also said that “No, it is not the time to abandon the BSC. The genic concept proposed by Wu goes against BSC but at the same time it has also been argued that none whole heartedly embraced the new genic concept of species. Recently, based on the work done on bacteria and viruses, it has been suggested that a single biological species definition once thought to be limited to sexually reproducing organisms, is applicable across all cellular and acellular life forms. Thus, there is a single universal definition of species across Life’s domain

The Tree Of Life: metaphysics vs. metaphor

A hundred years ago, in January 1904, E.B. Poulton gave an address entitled ‘What is a species?’ The resulting article, published in the Proceedings of the Entomological Society of London, is perhaps the first paper ever devoted entirely to a discussion of species concepts, and the first to elaborate what became known as the ‘biological species concept’. Poulton argued that species were syngamic (i.e. formed reproductive communities), the individual members of which were united by synepigony (common descent). Poulton's species concept was informed by his knowledge of polymorphic mimicry in Papilio butterflies: male and female forms were members of the same species, in spite of being quite distinct morphologically, because they belonged to syngamic communities. It is almost certainly not a coincidence that Alfred Russel Wallace had just given Poulton a book on mimicry in December 1903. This volume contained key reprints from the 1860s including the first mimicry papers, by Henry Walter Bates, Wallace himself and Roland Trimen. All these papers deal with species concepts and speciation as well as mimicry, and the last two contain the initial discoveries about mimetic polymorphism in Papilio: strongly divergent female morphs must belong to the same species as non‐mimetic males, because they can be observed in copula in nature. Poulton, together with his contemporaries Karl Jordan and Walter Rothschild, who had monographed world Papilionidae, were strongly influential on the evolutionary synthesis 40 years later. Ernst Mayr, in particular, had collected birds and butterflies for Walter Rothschild, and had visited Tring, where Jordan worked, in the 1920s. The recognition of different kinds of reproductive and geographic isolation, the classification of isolating mechanisms, the use of the term sympatry, and the biological species concept all trace back to Poulton's 1904 paper. Poulton's paper, in turn, inherits much from Wallace's 1865 paper on Asian Papilio contained in the very book Wallace gave Poulton a month earlier. Wallace's gift, and Poulton's subsequent New Year address are thus key events in the history of species concepts, systematics and evolutionary biology.

Abstractxxxxxx.

The Biological Species Concept (BSC) (Mayr, 1942) and more recent interpretations (Neigel & Avise, 1986; Moritz, 1994) attempt to define species in the context of an assumed evolutionary process; separated populations initially differ in gene frequency and then accumulate genetic differences until they become reproductively incompatible, at which point species status is achieved. Wu’s (2001) paper expands this scheme to the genic level: with longer time of separation, ever larger portions of the genome diverge to the point where selection prevents gene flow, until reproductive isolation affects all loci. The work of Wu and colleagues has greatly improved our understanding of the number and distribution of genes affecting reproductive differences. However, despite the widely shared excitement about these studies, we should consider carefully what they teach us about the process of speciation. Just as the BSC, Wu’s genic view implicitly assumes that speciation is a gradual build-up of divergence leading to reproductive isolation. This assumption of the BSC, however, is not justified, as it would predict a close correlation of genetic divergence and reproductive isolation and, at a deeper evolutionary level, that the closest relatives are less stringently reproductively isolated than more distantly related species. However, the correlation of sequence divergence and reproductive isolation is tenuous (Coyne & Orr, 1997), and many hybrid zones exist between species which are not each others’ sister (Cracraft, 1989). Therefore, the gradualist model underlying the BSC is poorly supported empirically, and reproductive isolation is not a suitable parameter to represent the historical (evolutionary) process which led to the existence of species (Cracraft, 1989). For the same reasons, the genic view may also suffer from the difficulty of linking the observed phenomenon (reproductive isolation) with the history of a lineage. To date, we have insufficient data to test whether there is a direct correlation of the number of speciation traits with increased phylogenetic divergence. Although the Drosophila melanogaster group data (Table 1 in Wu’s paper) seem to support this notion, they may be insufficient. First, the assignment of Stages seems rather arbitrary and in the case of the proposed Stages III and IV the number of differences in the comparisons may not be significant; hence the correlation of speciation loci with node level in the phylogeny may be weak. Secondly, even if there is a good correlation of the number of differentiated speciation loci with evolutionary divergence, these loci may have little to do with the speciation process itself but may be a trivial consequence of increasing divergence of cell components. For example, genes coding for rRNA could easily show up as speciation loci in the genetic screens if the gene products are too divergent for molecular interactions in cross-species genetic tests. The fact that the natural world is composed of species, i.e. discrete groups of organisms which are recognizably different from other such groups, argues against a view (also promoted by Wu) that species are simply peaks (adaptive or otherwise) in a continuum of variation. Sometimes discrete groups may be difficult to detect because of the lack of diagnostic features, because divergence is very shallow, or because there is in fact some level of gene flow, but the observation of discrete species holds in principle throughout the animal kingdom. Hence, species and the process of speciation should not be viewed primarily as quantitative phenomena. Speciation may be sudden and more consistent with a punctuated process, and may be independent of the level of divergence. In particular under allopatric scenarios, speciation may involve the disruption of continuously distributed groups through extinction of populations in some parts of the range (Nixon & Wheeler, 1992; Vogler, 1998). If, as proposed by Wu, speciation loci are driving the rest of the genome to complete isolation this will require prolonged interactions of gene pools for selection to act. Wu’s proposed model therefore may be most appropriate for sympatric and parapatric scenarios. But as evidence is mounting for a mostly allopatric mode of speciation in animals (Barraclough & Vogler, 2000) the assumption of interactions of differentiated populations may not be realistic, even for the D. melanogaster group. Without the interactions, speciation genes and marker loci should have largely the same history and the proposed differences in both sets of loci may not be detectable. The critical issue, as pointed out by Wu, will be to determine the degree to which selection plays a role in generating and maintaining species-level differences. Finally, the analysis of species-level differences, including those of speciation genes, requires that entities can be clearly defined when these comparisons are made. The genic view does not address the question of how to define what is a species (e.g. why are the D. melanogaster Z and M groups ‘races’, not ‘species’?) and what is their extent (e.g. which populations should be considered part of either race?). Traditionally, insect species have been separated on the basis of diagnostic traits. Under the phylogenetic species concept (PSC) a marker present in all individuals of a (group of) population(s), but not present in any other groups, is taken as a proxy to define a distinct gene pool. It is comforting that the study of genic differences revealed extensive divergence in speciation genes between D. simulans and D. melanogaster which are clearly definable by diagnostic differences (but not necessarily by the criterion of reproductive isolation). This suggests that the usual way of separating species by diagnosis is a valid operational procedure for discovering subdivided gene pools. Therefore, the possibly most exciting result of the high-resolution genetic analysis is that it provides a more profound empirical basis for the application of pattern based concepts to define species, no matter which process led to their speciation.

The phylogenetic species concept is applied for the first time to a major radiation of birds, the birds-of-paradise (Paradisaeidae) of Australasia. Using the biological species concept, previous workers have postulated approximately 40-42 species in the family. Of these, approximately 13 are monotypic and 27 are polytypic with about 100 subspecies. Phylogenetic species are irreducible (basal) clusters of organisms (terminal taxa) that are diagnosably distinct from other such clusters. Within the context of this concept, approximately 90 species of paradisaeids are postulated to have diversified within Australasia. The phylogenetic species concept more accurately describes evolutionary diversity within the family and provides a better theoretical and empirical framework for analysing speciation, historical biogeography and patterns of morphological, behavioral and ecological diversification within this group than does the biological species concept.

Species of malaria parasite (phylum Apicomplexa: genus Plasmodium) have traditionally been described using the similarity species concept (based primarily on differences in morphological or life-history characteristics). The biological species concept (reproductive isolation) and phylogenetic species concept (based on monophyly) have not been used before in defining species of Plasmodium. Plasmodium azurophilum, described from Anolis lizards in the eastern Caribbean, is actually a two-species cryptic complex. The parasites were studied from eight islands, from Puerto Rico in the north to Grenada in the south. Morphology of the two species is very similar (differences are indistinguishable to the eye), but one infects only erythrocytes and the other only white blood cells. Molecular data for the cytochrome b gene reveal that the two forms are reproductively isolated; distinct haplotypes are present on each island and are never shared between the erythrocyte-infecting and leucocyte-infecting species. Each forms a monophyletic lineage indicating that they diverged before becoming established in the anoles of the eastern Caribbean. This comparison of the similarity, biological and phylogenetic species concepts for malaria parasites reveals the limited value of using only similarity measures in defining protozoan species.

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.

Fusarium isolates that form part of the Gibberella fujikuroi species complex have been classified using either a morphological, biological, or phylogenetic species concept. Problems with the taxonomy of Fusarium species in this complex are mostly experienced when the morphological and biological species concepts are applied. The most consistent identifications are obtained with the phylogenetic species concept. Results from recent studies have presented an example of discordance between the biological and phylogenetic species concepts, where a group of F. subglutinans sensu stricto isolates, i.e., isolates belonging to mating population E of the G. fujikuroi complex, could be sub-divided into more than one phylogenetic lineage. The aim of this study was to determine whether this sub-division represented species divergence or intraspecific diversity in F. subglutinans. For this purpose, we included 29 F. subglutinans isolates belonging to the E-mating population that were collected from either maize or teosinte, from a wide geographic range. DNA sequence data for six nuclear regions in each of these isolates were obtained and used in phylogenetic concordance analyses. These analyses revealed the presence of two major groups representing cryptic species in F. subglutinans. These cryptic species were further sub-divided into a number of smaller groups that appear to be reproductively isolated in nature. This suggests not only that the existing F. subglutinans populations are in the process of divergence, but also that each of the resulting lineages are undergoing separation into distinct taxa. These divergences did not appear to be linked to geographic origin, host, or phenotypic characters such as morphology.

Fusarium isolates that form part of the Gibberella fujikuroi species complex have been classified using either a morphological, biological, or phylogenetic species concept. Problems with the taxonomy of Fusarium species in this complex are mostly experienced when the morphological and biological species concepts are applied. The most consistent identifications are obtained with the phylogenetic species concept. Results from recent studies have presented an example of discordance between the biological and phylogenetic species concepts, where a group of F. subglutinans sensu stricto isolates, i.e., isolates belonging to mating population E of the G. fujikuroi complex, could be sub-divided into more than one phylogenetic lineage. The aim of this study was to determine whether this sub-division represented species divergence or intraspecific diversity in F. subglutinans. For this purpose, we included 29 F. subglutinans isolates belonging to the E-mating population that were collected from either maize or teosinte, from a wide geographic range. DNA sequence data for six nuclear regions in each of these isolates were obtained and used in phylogenetic concordance analyses. These analyses revealed the presence of two major groups representing cryptic species in F. subglutinans. These cryptic species were further sub-divided into a number of smaller groups that appear to be reproductively isolated in nature. This suggests not only that the existing F. subglutinans populations are in the process of divergence, but also that each of the resulting lineages are undergoing separation into distinct taxa. These divergences did not appear to be linked to geographic origin, host, or phenotypic characters such as morphology.

Oh, what a tangled web we weave

Speciation has been termed Darwin’s mystery of mysteries. I suggest that whether speciation is deemed mysterious is species-concept dependent. I review speciation under the biological species concept (BSC) and the phylogenetic species concept (PSC) with a focus on the geography and evolutionary processes of avian speciation. In birds, the dominant geographic mode is allopatry. Under a BSC, speciation requires intrinsic reproductive isolation between taxa, an epiphenomenon, a process that has appeared mysterious because of the varied ways reproductive isolation can arise between sister taxa. Using intrinsic reproductive isolation to rank taxa as species can lead to paraphyletic species taxa, which are inappropriate for evolutionary and comparative studies. In the PSC, speciation involves the evolution of diagnostic characteristics between allopatric populations via genetic or phenotypic drift, natural selection, and sexual selection, which are not mysterious. Here I place pairs of New World warblers along a speciation continuum, which revealed that some species currently considered biological species are actually phylogenetic species that retain the ancestral ability to hybridize. A BSC and PSC classification of Galapagos finches reveals differences owing to hybridization. Any study of speciation should declare a species concept, criteria for recognizing species, and a research program to identify processes of lineage divergence or reproductive isolation.