Species concepts and species delimitation

The issue of species delimitation has long been confused with that of species conceptualization, leading to a half century of controversy concerning both the definition of the species category and methods for inferring the boundaries and numbers of species. Alternative species concepts agree in treating existence as a separately evolving metapopulation lineage as the primary defining property of the species category, but they disagree in adopting different properties acquired by lineages during the course of divergence (e.g., intrinsic reproductive isolation, diagnosability, monophyly) as secondary defining properties (secondary species criteria). A unified species concept can be achieved by treating existence as a separately evolving metapopulation lineage as the only necessary property of species and the former secondary species criteria as different lines of evidence (operational criteria) relevant to assessing lineage separation. This unified concept of species has several consequences for species delimitation, including the following: First, the issues of species conceptualization and species delimitation are clearly separated; the former secondary species criteria are no longer considered relevant to species conceptualization but only to species delimitation. Second, all of the properties formerly treated as secondary species criteria are relevant to species delimitation to the extent that they provide evidence of lineage separation. Third, the presence of any one of the properties (if appropriately interpreted) is evidence for the existence of a species, though more properties and thus more lines of evidence are associated with a higher degree of corroboration. Fourth, and perhaps most significantly, a unified species concept shifts emphasis away from the traditional species criteria, encouraging biologists to develop new methods of species delimitation that are not tied to those properties.     

Species concepts and the ontology of evolution

Biologists and philosophers have long recognized the importance of species, yet species concepts serve two masters, evolutionary theory on the one hand and taxonomy on the other. Much of present-day evolutionary and systematic biology has confounded these two roles primarily through use of the biological species concept. Theories require entities that are real, discrete, irreducible, and comparable. Within the neo-Darwinian synthesis, however, biological species have been treated as real or subjectively delimited entities, discrete or nondiscrete, and they are often capable of being decomposed into other, smaller units. Because of this, biological species are generally not comparable across different groups of organisms, which implies that the ontological structure of evolutionary theory requires modification. Some biologists, including proponents of the biological species concept, have argued that no species concept is universally applicable across all organisms. Such a view means, however, that the history of life cannot be embraced by a common theory of ancestry and descent if that theory uses species as its entities.These ontological and biological difficulties can be alleviated if species are defined in terms of evolutionary units. The latter are irreducible clusters of reproductively cohesive organisms that are diagnosably distinct from other such clusters. Unlike biological species, which can include two or more evolutionary units, these phylogenetic species are discrete entities in space and time and capable of being compared from one group to the next.     

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.     

(New) Species concepts,species delimitation and the inherent limitations of taxonomy

The species problem, despite decades of heated debates, has not been resolved yet. Recently, two new species concepts have been published, the mitonuclear compatibility species concept and the inclusive species concept. I briefly discuss them, together with a recent attempt at standardizing taxonomic decisions, in the broader framework of what I believe is an inherent limitation of taxonomy—imposing a discrete system on a continuous process (evolution) that leads to fuzzy boundaries in nature. In the light of this, taxonomists, biologists in general and conservationists alike will have to accept the fact that completely nonarbitrary species delimitation is impossible. This has serious ramifications in all disciplines that rely on species, and particularly species counts, as a basic currency for quantitative analyses (ecology, evolutionary biology) and practical decision-making (conservation and environmental policy).     

Ontogeny,auditory structures,and primate evolution

The anatomy of the auditory region, particularly the carotid circulatory patterns and ectotympanic-petrosal relationships, has played a prominent role in primate systematics and phylogenetic reconstructions. Ontogenetic stages of petrosal-ectotympanic relationship are presented for certain strepsirhines. It is suggested that the “ectotympanic tube” or “ossified annulus membrane” found in early Tertiary primates is not necessarily an homologous structure to the true ectotympanic tube seen in haplorhines, and thus cannot be considered a shared, derived feature linking known Paleogene primates from Europe or North America to tarsioid and/or anthropoid ancestry. No fossil primate yet discovered makes a convincing ancestor for the earliest known anthropoids from the Oligocene of Africa. This is probably due to the fact that it still lies undiscovered in the Paleogene of Africa.     

Raptors and primate evolution

Most scholars agree that avoiding predators is a central concern of lemurs, monkeys, and apes. However, given uncertainties about the frequency with which primates actually become prey, the selective importance of predation in primate evolution continues to be debated. 1 - 9 Some argue that primates are often killed by predators, 5 , 6 while others maintain that such events are relatively rare. 2 , 7 , 9 Some authors have contended that predation's influence on primate sociality has been trivial 10 , 11 ; others counter that predation need not occur often to be a powerful selective force. 12 - 14 Given the challenges of documenting events that can be ephemeral and irregular, we are unlikely ever to amass the volume of systematic, comparative data we have on such topics as feeding, social dynamics, or locomotor behavior. Nevertheless, a steady accumulation of field observations, insight gained from natural experiments, and novel taphonomic analyses have enhanced understanding of how primates interact with several predators, especially raptors, the subject of this review.     

Predation and primate evolution

This paper presents the results of a general review of predation on nonhuman primates as a selective force in primate evolution. Testable hypotheses derived from the literature on predation on primates, concerning sexual dimorphism, male defense, group size, solitaries, transfer, subgrouping, and sex ratio, were applied to the available data on populations with varying predation rates in search of significant correlations. All seven hypotheses were supported, indicating that predation is and has been an important determinant of primate evolutionary history. Suggestions for accumulating a larger and more accurate body of information on predation rates on primates are offered.     

Retroviruses and primate evolution

Human endogenous retroviruses (HERVs), probably representing footprints of ancient germ-cell retroviral infections, occupy about 1% of the human genome. HERVs can influence genome regulation through expression of retroviral genes, either via genomic rearrangements following HERV integrations or through the involvement of HERV LTRs in the regulation of gene expression. Some HERVs emerged in the genome over 30 MYr ago, while others have appeared rather recently, at about the time of hominid and ape lineages divergence. HERVs might have conferred antiviral resistance on early human ancestors, thus helping them to survive. Furthermore, newly integrated HERVs could have changed the pattern of gene expression and therefore played a significant role in the evolution and divergence of Hominoidea superfamily. Comparative analysis of HERVs, HERV LTRs, neighboring genes, and their regulatory interplay in the human and ape genomes will help us to understand the possible impact of HERVs on evolution and genome regulation in the primates. BioEssays 22:161-171, 2000.     

Integration, individuality and species concepts

Integration (interaction among parts of an entity) is suggested to be necessary for individuality (contra, Metaphysics and the Origin of Species). A synchronic species is an integrated individual that can evolve as a unified whole; a diachronic lineage is a non-integrated historical entity that cannot evolve. Synchronic species and diachronic lineages are consequently suggested to be ontologically distinct entities, rather than alternative perspectives of the same underlying entity (contra Baum (1998), Syst. Biol. 47, 641–653; de Queiroz (1995), Endless Forms: Species and Speciation, pp. 57–75; Genes, Categories and Species). Species concepts usually refer to either one or the other entity; for instance, the Biological Species Concept refers to synchronic species, whereas the Cladistic Species Concept refers to diachronic lineages. The debate over species concepts has often failed to recognise this distinction, resulting in invalid comparisons between definitions that attempt to delineate fundamentally different entities. This revised version was published online in July 2006 with corrections to the Cover Date.     

Inbreeding,kin selection,and primate social evolution

In this paper I argue (a) that the study of kin selection may be facilitated by looking for influences of inbreeding, which is an important aspect of a population's genetic structure; (b) that in nonhuman primates the level of inbreeding will be largely a function of the rate of migration by individuals, usually only of one sex, between social units or troops; (c) that many primate species live in relatively outbred groups, and that their social structure reflects this; and (d) that extensive social contrasts between bonnet and pigtail macaques reflect evolution by kin selection under different levels of inbreeding.     

Genes,development, and evolvability in primate evolution

Development is the process whereby a fertilized cell becomes a mature individual. In metazoans, this complex process involves the differentiation of somatic cells into committed cell and tissue types; the organization and migration of cells, tissues, and anatomical structures relative to one another; and growth. 1 Development matters to evolution in two ways. First, development carries out heritable genetic instructions contained in zygotes to produce functioning yet phenotypically varied individuals. At the population level, this variation in form and function among individuals provides the “raw material” for evolution. Second, the mechanisms of development influence the magnitude, direction, and interdependence of heritable phenotypic variation among traits. Together with phenomena such as genetic drift, organismal development determines the raw material available to selection and thus influences the rate and direction of phenotypic evolution. 2 , 3     

Species concepts and phylogenetics

Concepts of species proposed within the phylogenetic paradigm arecritically reviewed. Most so called phylogenetic species concepts relyheavily on factors immaterial to phylogenetic hypotheses. Thus, theyhave limited empirical content and offer weak bases on which to makedecisions about real problems related to species. Any workable notion ofspecies relies on an explicit character analysis, rather than onabstract properties of lineages, narrative predications and speculationson tokogenetic relationships. Species only exist conjecturally, as thesmallest meaningful units for phylogenetic analysis, as based oncharacter evidence. Such an idea considers species to be conjecturesbased on similarity, that are subsequently subject to testing by theresults of analysis. Species, thus, are units of phylogenetic analysisin the same way as hypotheses of homology are units of comparablesimilarities, i.e. conjectures to be tested by congruence. Althoughmonophyly need not be demonstrated for species-level taxa, hypotheses ofrelationships are the only basis to refute species limits and guidenecessary rearrangements. The factor that leads to recognition ofspecies is similarity in observed traits. The concept of life cycle isintroduced as an important element in the discussion of species, as anefficient way to convey subsidiary notions of sexual dimorphism,polymorphism, polytypy and clusters of diagnosable semaphoronts. Thenotion of exemplars is used to expand the concept ofspecies-as-individual-organisms into a more generally usable concept.Species are therefore proposed for a diagnosable sample of(observed or inferred) life cycles represented by exemplars all of whichare hypothesized to attach to the same node in a cladogram, and whichare not structured into other similarly diagnosable clusters. Thisdefinition is character-based, potentially testable by reference to abranching diagram, and dispenses with reference to ancestor-descendantrelationships or regression into population concepts. It provides aworkable basis on which to proceed with phylogenetic analysis and abasis for that analysis to refute or refine species limits. A protocolis offered for testing hypotheses of species boundaries in cladograms.