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.     

On the reality and recognisability of asexual organisms: morphological analysis of the masticatory apparatus of bdelloid rotifers

Species concepts and definitions have been a long-standing debate in evolutionary biology since before Darwin, and almost all proposed solutions are based upon grouping and clustering, with species conceived as somehow biological distinct entities, originated and maintained mainly by reproductive isolation. Lacking reproductive exchange, asexual organisms such as bdelloid rotifers, the best-supported clade of so-called 'ancient asexuals', pose an interesting challenge to debates over the reality of species. However, few data are available on bdelloid rotifers. The only evidence has been that bdelloid species have been more consistently recognised than in their sister sexual group, the monogonont rotifers, across successive taxonomic treatments, but this is confounded by the much lesser degree of taxonomic interest in bdelloids. We applied geometric morphometrics analyses on shape and size of hard masticatory pieces, named trophi, of 1420 bdelloids, belonging to 48 populations of eight traditional species, to test the hypothesis of recognisability of bdelloids. Our morphological analysis confirms that traditional bdelloid species are separated distinct entities, possessing trophi morphologies divided by gaps between taxa, similar to patterns of morphological features in sexually reproducing organisms. In common with most microscopic understudied organisms, bdelloid rotifers harbour much previously undescribed diversity: we found significant differences in trophi morphology within traditional species, revealing the existence of cryptic taxa, similar to those also found in facultatively sexual monogonont rotifers. We confirm that recognisability in bdelloids is not qualitatively different from other small understudied animals such as monogononts, and that sexual versus asexual reproduction does not lead to differences in morphological diversity patterns, as previously suggested based on interpretation of taxonomic revisions.     

How to be a chaste species pluralist-realist: the origins of species modes and the synapomorphic species concept

The biological species (biospecies) concept applies only to sexually reproducing species, which means that until sexual reproduction evolved, there were no biospecies. On the universal tree of life, biospecies concepts therefore apply only to a relatively small number of clades, notably plants andanimals. I argue that it is useful to treat the various ways of being a species (species modes) as traits of clades. By extension from biospecies to the other concepts intended to capture the natural realities of what keeps taxa distinct, we can treat other modes as traits also, and so come to understand that theplurality of species concepts reflects the biological realities of monophyletic groups.We should expect that specialists in different organisms will tend to favour those concepts that best represent the intrinsic mechanisms that keep taxa distinct in their clades. I will address the question whether modes ofreproduction such as asexual and sexual reproduction are natural classes, given that they are paraphyletic in most clades.     

Sperm-dependent parthenogens delay the spatial expansion of their sexual hosts

It has been known for long time that asexual organisms may affect the distribution of sexual taxa. In fact, such phenomenon is inherent in the concept of geographical parthenogenesis. On the other hand, it was generally hypothesized that sperm-dependent asexuals may not exercise the same effect on related sexual population, due to their dependence upon them as sperm-donors. Recently, however, it became clear that sperm-dependent asexuals may directly or indirectly affect the distribution of their sperm-hosts, but rather in a small scale. No study addressed the large-scale biogeographic effect of the coexistence of such asexuals with the sexual species. In our study we were interested in the effect of sexual–asexual coexistence on the speed of spatial expansion of the whole complex. We expand previously published Lotka–Volterra model of the coexistence of sexual and gynogenetic forms of spined loach (Cobitis; Teleostei) hybrid complex by diffusion. We show that presence of sperm-dependent parthenogens is likely to negatively affect the spatial expansion of sexuals, and hence the whole complex, compared to pure sexual population. Given that most of the known sperm-dependent asexual complexes are distributed in areas prone to climate-induced colonization/extinction events, we conclude that such mechanism may be an important agent in determining the biogeography of sexual taxa and therefore requires further attention including empirical tests.     

Biological species is the only possible form of existence for higher organisms: the evolutionary meaning of sexual reproduction

   

Consistent holistic view of sexual species as the highest form of biological existence is presented. The Weismann's idea that sex and recombination provide the variation for the natural selection to act upon is dominated in most discussions of the biological meaning of the sexual reproduction. Here, the idea is substantiated that the main advantage of sex is the opposite: the ability to counteract not only extinction but further evolution as well. Living systems live long owing to their ability to reproduce themselves with a high fidelity. Simple organisms (like bacteria) reach the continued existence due to the high fidelity of individual genome replication. In organisms with a large genome and complex development, the achievable fidelity of DNA replication is not enough for the precise reproduction of the genome. Such species must be capable of surviving and must remain unchanged in spite of the continuous changes of their genes. This problem has no solution in the frame of asexual ("homeogenomic") lineages. They would rapidly degrade and become extinct or blurred out in the course of the reckless evolution. The core outcome of the transition to sexual reproduction was the creation of multiorganismic entity - biological species. Individual organisms forfeited their ability to reproduce autonomously. It implies that individual organisms forfeited their ability to substantive evolution. They evolve as a part of the biological species. In case of obligatory sexuality, there is no such a thing as synchronic multi-level selection. Natural selection cannot select anything that is not a unit of reproduction. Hierarchy in biology implies the functional predestination of the parts for the sake of the whole. A crucial feature of the sexual reproduction is the formation of genomes of individual organisms by random picking them over from the continuously shuffled gene pool instead of the direct replication of the ancestor's genome. A clear anti-evolutionary consequence of the sexuality is evident from the fact that the genotypes of the individuals with an enhanced competitiveness are not transmitted to the next generation. Instead, after mating with "ordinary" individuals, these genotypes scatter and rearrange in new gene combinations, thus preventing the winner from exploiting the success.     

Imitating the cost of males: A hypothesis for coexistence of all‐female sperm‐dependent species and their sexual host

All‐female sperm‐dependent species are particular asexual organisms that must coexist with a closely related sexual host for reproduction. However, demographic advantages of asexual over sexual species that have to produce male individuals could lead both to extinction. The unresolved question of their coexistence still challenges and fascinates evolutionary biologists. As an alternative hypothesis, we propose those asexual organisms are afflicted by a demographic cost analogous to the production of males to prevent exclusion of the host. Previously proposed hypotheses stated that asexual individuals relied on a lower fecundity than sexual females to cope with demographic advantage. In contrast, we propose that both sexual and asexual species display the same number of offspring, but half of asexual individuals imitate the cost of sex by occupying ecological niches but producing no offspring. Simulations of population growth in closed systems under different demographic scenarios revealed that only the presence of nonreproductive individuals in asexual females can result in long‐term coexistence. This hypothesis is supported by the fact that half of the females in some sperm‐dependent organisms did not reproduce clonally.     

ON GENETIC SEGREGATION AND THE EVOLUTION OF SEX

It has recently been argued that because the genetic load borne by an asexual species resulting from segregation, relative to a comparable sexual population, is greater than two, sex can overcome its twofold disadvantage and succeed. We evaluate some of the assumptions underlying this argument and discuss alternative assumptions. Further, we simulate the dynamics of competition between sexual and asexual types. We find that for populations of size 100 and 500 the advantages of segregation do not outweigh the cost of producing males. We conclude that, at least for small populations, drift and the cost of sex govern the evolution of sexuality, not selection or segregation. We believe, however, that if sexual and asexual populations were isolated for a sufficiently long period, segregation might impart a fitness advantage upon sexuals that could compensate for the cost of sex and allow sexuals to outcompete asexuals upon their reunion.     

AN AMPLIFICATION OF THE PHYLOGENETIC SPECIES CONCEPT

Abstract— The goal of a phylogenetic species concept is to reveal the smallest units that are analysable by cladistic methods and interpretable as the result of phylogenctic history. We define species as the smallest aggregation of populations (sexual) or lineagcs (asexual) diagnosable by a unique combination of character states in comparable individuals (semaphoronts). A character state is an inherited attribute distributed among all comparable individuals (semaphoronts) of the same historical population, clade, or terminal lineage. This definition of species is character-based and pattern oriented. Evolutionary explanations of phylogenetic species are consistent with contemporary explanations of processes of speciation, but require only the assumption of nested hierarchical pattern. We discuss the compatibility of the phylogenetic species concept with various biological needs for species and justify its use at the exclusion of alternative species concepts.     

LARGE POPULATION SIZE PREDICTS THE DISTRIBUTION OF ASEXUALITY IN SCALE INSECTS

Understanding why some organisms reproduce by sexual reproduction while others can reproduce asexually remains an important unsolved problem in evolutionary biology. Simple demography suggests that asexuals should outcompete sexually reproducing organisms, because of their higher intrinsic rate of increase. However, the majority of multicellular organisms have sexual reproduction. The widely accepted explanation for this apparent contradiction is that asexual lineages have a higher extinction rate. A number of models have indicated that population size might play a crucial role in the evolution of asexuality. The strength of processes that lead to extinction of asexual species is reduced when population sizes get very large, so that the long‐term advantage of sexual over asexual reproduction may become negligible. Here, we use a comparative approach using scale insects (Coccoidea, Hemiptera) to show that asexuality is indeed more common in species with larger population density and geographic distribution and we also show that asexual species tend to be more polyphagous. We discuss the implication of our findings for previously observed patterns of asexuality in agricultural pests.     

What is complexity?

Arguments for or against a trend in the evolution of complexity are weakened by the lack of an unambiguous definition of complexity. Such definitions abound for both dynamical systems and biological organisms, but have drawbacks of either a conceptual or a practical nature. Physical complexity, a measure based on automata theory and information theory, is a simple and intuitive measure of the amount of information that an organism stores, in its genome, about the environment in which it evolves. It is argued that physical complexity must increase in molecular evolution of asexual organisms in a single niche if the environment does not change, due to natural selection. It is possible that complexity decreases in co-evolving systems as well as at high mutation rates, in sexual populations, and in time-dependent landscapes. However, it is reasoned that these factors usually help, rather than hinder, the evolution of complexity, and that a theory of physical complexity for co-evolving species will reveal an overall trend towards higher complexity in biological evolution.     

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.     

General environmental heterogeneity as the explanation of sexuality? Comparative study shows that ancient asexual taxa are associated with both biotically and abiotically homogeneous environments

Ecological theories of sexual reproduction assume that sexuality is advantageous in certain conditions, for example, in biotically or abiotically more heterogeneous environments. Such theories thus could be tested by comparative studies. However, the published results of these studies are rather unconvincing. Here, we present the results of a new comparative study based exclusively on the ancient asexual clades. The association with biotically or abiotically homogeneous environments in these asexual clades was compared with the same association in their sister, or closely related, sexual clades. Using the conservative definition of ancient asexuals (i.e., age >1 million years), we found eight pairs of taxa of sexual and asexual species, six differing in the heterogeneity of their inhabited environment on the basis of available data. The difference between the environmental type associated with the sexual and asexual species was then compared in an exact binomial test. The results showed that the majority of ancient asexual clades tend to be associated with biotically, abiotically, or both biotically and abiotically more homogeneous environments than their sexual controls. In the exploratory part of the study, we found that the ancient asexuals often have durable resting stages, enabling life in subjectively homogeneous environments, live in the absence of intense biotic interactions, and are very often sedentary, inhabiting benthos, and soil. The consequences of these findings for the ecological theories of sexual reproduction are discussed.     

Species concepts in agamic complexes: Applications in theRanunculus auricomus complex and general perspectives

The application of different current species concepts to the predominantly apomicticR. auricomus complex (goldilocks) is discussed. As with other uniparental reproducing organisms, biological species concepts are hardly applicable in apomictic groups. Information on reproductive systems, phenetic and ecological differentation, and evolutionary traits favour an “agamospecies” concept. It is argued that agamic lineages in goldilocks can be treated neither as subspecific taxa, nor as hybrids. A general viewpoint is proposed that species are stable phases within a continuous process of diversification of ancestral-descendent lineages. Constancy of progeny, similarity of phenotype, and ecogeographical niches of organisms are regarded as the most important operational criteria for grouping and ranking of species. Mode of reproduction is seen as a feature of a species — not as a criterion for its definition. Internal stability of features is regarded as more important for species definition than the features themselves.     

Comparison of the evolutionary distances among syngens and sibling species of Paramecium

The morphospecies of the genus Paramecium have several mating type groups, so-called syngens, composed of cells of complementary mating types. The Paramecium aurelia complex is composed of 15 sibling species assigned to the species from the syngen. To increase our understanding of the evolutionary relationships among syngen and sibling species of the genus Paramecium, we investigated the gene sequences of cytosol-type hsp70 from 7 syngens of Paramecium caudatum and 15 sibling species of P. aurelia. Molecular phylogenetic trees indicated that the P. aurelia complex could be divided into four lineages and separated into each sibling species. However, we did not find any obvious genetic distance among syngens of P. caudatum, and they could only be separated into two closely related groups. These results indicated that the concept of syngens in P. caudatum differs quite markedly from that of the P. aurelia complex. In addition, we also discuss the relationships among these species and other species, Paramecium jenningsi and Paramecium multimicronucleatum, which were once classified as varieties of P. aurelia.     

Why the Phylogenetic Species Concept?—Elementary

Although species play a number of unique and necessary roles in biology, none are more important than as the elements of phylogeny, nomenclature, and biodiversity study. Species are not divisible into any smaller units among which shared derived characters can be recognized with fidelity. Biodiversity inventory, assessment, and conservation are dependent upon a uniformly applicable species concept. Species are the fundamental units in formal Linnaean classification and zoological nomenclature. The Biological Species Concept, long given nominal support by most zoologists, forced an essentialy taxonomic problem (what are species?) into a population genetics framework (why are there species?). Early efforts at a phylogenetic species concept focused on correcting problems in the Biological Species Concept associated with ancestral populations, then applying phylogenetic logic to species themselves. Subsequently, Eldredge and Cracraft, and Nelson and Platnick, each proposed essentially identical and truly phylogenetic species concepts that permitted the rigorous recognition of species prior to and for the purposes of phylogenetic analysis, yet maintained the integrity of the Phylogenetic Species Concept outside of cladistic analysis. Such phylogenetic elements have many benefits, including giving to biology a unit species concept applicable across all kinds of living things including sexual and asexual forms. This is possible because the Phylogenetic Species Concept is based on patterns of character distributions and is therefore consistent with the full range of possible evolutionary processes that contribute to species formation, including both biotic and abiotic (even random) factors.     

Thermal aspects of electromagnetic field interactions with bound calcium ions at the nerve cell surface

This paper examines the cost of meiosis in a species with an alternation of sexual and asexual generations (e.g. Daphnia), by means of calculations of the survival probabilities of mutant genes causing patterns of wholly asexual reproduction. It is shown that the survival probabilities of such mutations are lower with an alternation of sexual and asexual generations than with an initial population which reproduces exclusively sexually. The survival probabilities decrease as the number of asexual generations within each reproductive cycle increases. It is argued that these results imply a lower than usual cost of meiosis when there is an alternation of generations, and that asexual reproduction cannot simply be equated with vegetative growth of a single multicellular organism.     

Population genetics of nonclonal, nonrandomly mating malaria parasites

In a highly controversial paper(1), Tibayrenc and colleagues have argued that clonal (asexual) reproduction may be a general phenomenon among protozoan parasites. Many parasitologists would be quite comfortable with a theory applied to Leishmania, Trypanosoma, Entamoeba and Giardia which proposes 'that uniparental reproduction is ... predominant enough in natural populations to generate clones that are stable in space and time ...' The current view is that these parasites can reproduce sexually some of the time (eg. Refs 2,3) but may not do so most of the time. What has provoked the most controversy(4-7) is the suggestion that malaria parasites can be considered as bedfellows of the above, for Plasmodium are generally thought to undergo obligate sexual reproduction in each generation. Here, Christopher Dye focuses on Tibayrenc's arguments for clonal reproduction in Plasmodium, not only because malaria parasites are at the heart of the dispute but also because an analysis of his arguments about sexually reproducing parasites carries implications for his assertions in general.     

Asexual plants change just as often and just as fast as do sexual plants when introduced to a new range

Some of the world's most economically and environmentally damaging introduced species reproduce asexually. While sexually reproducing introduced herbs have proven capable of rapid evolution, no previous study has quantified morphological changes in multiple obligatory asexually reproducing introduced species, or asked whether their potential for change differs from that of sexual species. We measured herbarium specimens of eight asexual species introduced to Australia and/or New Zealand. We quantified changes in leaf area, leaf shape, leaf mass per area, plant height and internode length through time since the species’ introduction. Half of the asexual species demonstrated significant change in at least one trait. The observed changes were substantial – up to 561% per 100 years. The proportion of species showing at least one significant morphological change did not differ significantly between our asexual species, and data measured in the same manner for 34 sexually reproducing introduced species. There was also no significant difference in the rate of morphological change in sexual versus asexual species. That is, we found that sexual species have not changed more often, or more quickly than their asexual counterparts. Our results show that asexually reproducing species can undergo rapid morphological change at a rate matching that of sexually reproducing species when introduced to a new range. Our results also suggest that asexually reproducing plants may be able to respond to changing conditions better than was previously appreciated.