Select all types of characters that are often used to compare species and construct cladograms.

I.C. Groups

Cladistics recognizes only monophyletic groups of organisms, which are those based on synapomorphies. Monophyletic groups are the only groups that can be circumscribed by objective boundaries. In evolutionary terms, monophyletic groups comprise the most recent common ancestor and all of its descendants. In Fig. 2, Amniota, Tetrapoda, Osteichthyes, and Gnathostomata are all monophyletic. Two other types of “groups” are sometimes referred to but these are not groups in the same sense as monophyletic groups. Paraphyletic “groups” are based on symplesiomorphy; in evolutionary terms, their members are linked by common ancestry but one or more of the descendants of the most recent common ancestor are excluded. In Fig. 2, Pisces (fishes) is a paraphyletic assemblage. Many taxa traditionally regarded as ancestral, such as fishes, reptiles, and green algae, are paraphyletic. Polyphyletic “groups” are based on homoplasy, that is, characters that are considered convergently derived and that cannot be inferred to have been present in the most recent common ancestor of the included taxa. In Fig. 2, an assemblage comprising the dogfish and the turkey (perhaps based on the observation that both lay eggs surrounded by a shell, although no one would claim such a homology) would be a polyphyletic group.

Component Analysis

Cladistic biogeography would be uncomplicated if all groups of organisms were each represented by one taxon in each of the smallest identifiable areas of endemism. This is not the case. Unique patterns may be meaningful and cannot at the same time be incongruent with patterns determined from other taxa. Nevertheless, incongruence between two or more cladograms can occur for a variety of historical reasons. Particular groups of organisms can exhibit older or younger patterns than the groups to which they are being compared. Also, some taxa have dispersed and become widespread and by so doing have obscured the historical signal in the area patterns. Comparing several different groups of organisms is redundant in the sense that the same pattern is repeated over and over or areas are represented by two or more taxa. With extinction the observed pattern creates a spurious historical signal. All of these problems effectively cause sampling errors and lead to wrong predictions of the general patterns of area interrelationship. Nelson and Platnick (1981) used cladistic logic and component analysis to make comparisons between area cladograms to yield the maximum resolution in the general-area cladograms (see Box 1).

Box 1

Component analysis

To determine the degree of congruence between different groups of organisms occupying similar areas, the problems of ‘‘missing areas,’’ widespread taxa, and redundancy are taken into consideration using component analysis and consensus.

Components are the elements of a group of areas, or group of taxa, as determined by the branching pattern of a cladogram. For example, in a group comprising three taxa (or areas) A, B, and C, when B is more closely related to C, there are two components, a general uninformative ABC component and an informative BC component.

Components of cladograms in vicariance biogeography can be manipulated to extract historical signal from even the most recalcitrant cases (Figure 11). For example, consider the four areas of endemism, South Africa (SA), Pacific South America (PSA), New Zealand (NZ), and eastern Australia (EA). Now consider three groups of organisms distributed in these four areas; three species of lizards (L1–L3) in SA, PSA, and NZ, and three species each of birds (B1–B3) and fish (F1–F3) in PSA, NZ, and EA. The three numbered informative nodes (1–3) on the cladograms express the relationships for each species in the lizards, birds, and fishes. Notice that each group of organisms occurs in three areas, and in each case there is one area not present (EA for the lizards and SA for the birds and fish). Also, for each group there is one species endemic to an area, i.e., L2 in PSA, B2 in NZ, and F2 in EA. The remaining species are more widespread, occurring in either two or three areas (respectively L1, B1, and F1 in two areas and L3, B3, and F3 in three areas).

Because of widespread species and the lack of representation of one area in each of the area cladograms, at first sight relationships between the four areas seem difficult to resolve (Figure 11). However, it can be assumed that each species originated in one area with extinction, dispersal, and failures to vicariate, causing the more complex patterns. Taking this view, we can examine the informative three-area relationships in the area cladograms to see if they tell us anything about the general-area relationships. Thus, in the lizard cladogram, L1 in SA, L2 in NZ, and L3 in PSA is the only informative statement that can be represented as SA(PSA, NZ) and scored as 0(1, 1) in a matrix (Table 1, column 1). The ‘‘missing’’ area (EA) is scored as a dash. Informative area statements for birds are PSA(NZ, EA) and EA(NZ, PSA), and for fishes PSA(EA, NZ) and NZ(EA, PSA) similarly scored in the matrix (Table 1, columns 2–5). Consequently, for the three cladograms there are five informative three-area statements (Table 1). By using a standard parsimony analysis, the best fitting tree for the five statements is shown in Figure 12. Thus, despite the complexity of the patterns in the original three groups (Figure 11), if there is one history that best explains the data, then it might be a vicariance hypothesis for the four areas as offered in Figure 12—(SA, PSA, NZ, EA) (SA(PSA, NZ, EA)) (SA(PSA(NZ, EA)))—and shown as an area cladogram in Figure 13, indicating the relationships of the four areas of endemism.

Classification

Cladistic analysis shows that Class Trilobita is not primitive in relation to other early arachnomorph arthropods, and the trilobites are taken to be a natural group characterized by the calcified exoskeleton and ocular surface, the facial sutures, and features of the hypostome and pygidium. However, a comprehensive natural classification of the trilobites has not yet been devised. Thousands of genera have been grouped into hundreds of subfamilies and families, but the content and limits of many of these are subjective, and it is debated how they should be grouped into higher categories. Several major natural groups are widely accepted, especially amongst the post-Cambrian trilobites, but the origins of some of them are cryptic and how the various groups are inter-related remains uncertain. Obstacles to classification have included the relatively poor knowledge of the ontogenies of many trilobites, their limbs (and ventral features generally), the tendency for iterative evolutionary trends to yield misleading homeomorphic forms, and the unresolved questions that surround the great mass of plesiomorphic taxa in the Cambrian. None the less, great advances in the description and interpretation of trilobites in the latter half of the twentieth century has led to an improved understanding of the problems, and has yielded such provisional classifications as that presented in outline in Table 1. Cladistic and morphological analyses have provided some unexpected, although fundamentally satisfying, results, e.g., the transfer of the trinucleid group to the Asaphida.

Table 1. Major orders and suborders of trilobites. Some examples are shown in Figure 17

Classification

Cladistic analysis shows that Class Trilobita is not primitive in relation to other early arachnomorph arthropods, and the trilobites are taken to be a natural group characterized by the calcified exoskeleton and ocular surface, the facial sutures, and features of the hypostome and pygidium. However, a comprehensive natural classification of the trilobites has not yet been devised. Thousands of genera have been grouped into hundreds of subfamilies and families, but the content and limits of many of these are subjective, and it is debated how they should be grouped into higher categories. Several major natural groups are widely accepted, especially amongst the post-Cambrian trilobites, but the origins of some of them are cryptic and how the various groups are interrelated remains uncertain. Obstacles to classification have included the relatively poor knowledge of the ontogenies of many trilobites, their limbs (and ventral features generally), the tendency for iterative evolutionary trends to yield misleading homeomorphic forms, and the unresolved questions that surround the great mass of plesiomorphic taxa in the Cambrian. None the less, great advances in the description and interpretation of trilobites in the latter half of the 20th century has led to an improved understanding of the problems, and has yielded such provisional classifications as that presented in outline in Table 1. Cladistic and morphological analyses have provided some unexpected, although fundamentally satisfying, results, for example, the transfer of the trinucleid group to the Asaphida. For many years the Suborder Agnostina was grouped with the Suborder Eodiscina in the Order Agnostida, as shown in Table 1; there is no doubt that the Eodiscina are trilobites. However, wonderfully preserved agnostids have been described and they show special features not shared with trilobites at large. Increasingly workers are inclined to detach the Agnostina from the Eodiscina and to place them in a class separate from the Trilobita.

Table 1. Major orders and suborders of trilobites.

Some examples are shown in Fig. 17.

Paraphyly and Monophyly in Cladistics

Cladistics demonstrates that grades are impossible to characterize as they do not express relationships between organisms. There is no way of knowing when one grade starts and another stops. How many characters along a branch are required before it is possible to draw a line and say that one side represents a lower grade and the other side a higher grade? Related to this question is how many taxa belong to a grade group?

Hennig (1996) described a method to implement evolution by common descent by reconstructing phylogenies based on assessments of speciation (cladogenesis) and transformation of characters (now known as cladistics; see Methods of Systematics, and Cladistics). His most important contribution was to offer a precise definition of relationship and a technique for those relations to be discovered. A minimum of three taxa is necessary to express a relationship. For example, in Figure 11a taxa B and C are more closely related to each other, than either is to A, because they share a common ancestor not shared by A. Cladistic analysis finds monophyletic groups on the basis of uniquely derived, shared characters (synapomophies).

Hennig showed that monophyletic groups are “natural groups,” that branching nodes expressed relations, and that synapomorphies are the only measurable quantities for determining pattern. Hence neither horizontal nor vertical branches (anagenesis) are meaningful for expressing relationships on cladograms or for the determination of groups. Vertical branches say nothing about time and the relative nesting of nodes on the cladogram provide only relative rather than absolute estimates of ordinal time. Relationships could just as easily be represented by nested sets or Venn diagrams (Figure 11b).

Cladograms are synapomorphy schemes, induced from the most parsimonious distribution of characters to show sister-group relationships. In Figure 12a, taxa B and C represent one sister group nested in larger sister group, A and B + C. Cladograms are different from phylogenetic trees because they rely entirely on empirical data, taxa, and characters. They express only the general branching pattern of life because that is all that is available from analysis of taxa and form. The strongest support for this idea is that many phylogenetic trees can be hypothesized for the same cladogram irrespective of branch length (Figures 12b–e). Consequently, anagenesis, ancestors, and ancestor-descendant relationships are not directly available from character analysis but require models of one kind or another to arrive at answers to questions of rates of divergence. Cladograms are different from phylograms or phylogenetic trees because they are isomorphic with the classification. Cladograms are consistent with name hierarchy and they can be recovered from written classifications. On the basis of this property, Hennig (1966) justifiably claimed that phylogenetic systematics provided the only truly general reference system consistent with the theory of evolution by common descent.

The task of systematics for Hennig was to understand natural relationships (monophyly, monophyletic groups) and rid the general reference system of polyphyly and paraphyly. Although there has been considerable proliferation in the methods and sources of information in systematics, the main effect has been to put intense effort into cladogenesis by the discovery of clades or monophyletic groups. For the past 25 years or so systematics has concentrated on determining the pattern of life from its earliest beginnings to the highest nodes on the tree, especially as a result of massive strides in molecular biology. Programs in pattern analysis range from the minutiae of phylogeography within species and populations to the discovery of monophyletic clades throughout the entire history of life. On the process side have been intense efforts to discern the rates of macroevolution by calibrating what is known about fossil history and morphological evolution with what is known about base substitution rates in ubiquitous molecules.

Summary

Cladistic analysis of the 10 shark genera in the order Lamniformes, on the basis of 23 dental characters, was carried out using a computer program (PAUP 3.1.1) to infer phylogenetic relationships within the group. Mitsukurina was selected as the outgroup, and a single most parsimonious cladogram was generated. This cladogram, supported by four different statistical methods for assessing tree robustness, showed the Odontaspididae (Carcharias plus Odontaspis) to be a primitive clade. The Lamnidae proved to be the most derived clade, with Carcharodon plus Lamna as a clade and Isurus as the sister taxon. Carcharodon showed several autapomorphic dental characters related to trophic adaptations. The placement of Megachasma plus Cetorhinus as a clade within this cladogram is considered dubious, because both taxa may have independently reduced their teeth as an adaptation for filter feeding, and hence lost many dental characters necessary for accurate phylogenetic assessment. The cladogram generated from this study is compared with several recent analyses of extant lamniform shark relationships.

Glossary

Cladistic

A classification based entirely on monophyletic taxonomic groupings within a phylogeny; taxonomic units that are paraphyletic or polyphyletic are rejected. A cladist is one who practices cladistics, usually in the sense of using parsimony to adjudicate between data from multiple characters in the construction of a cladogram, which is an estimate of the true phylogeny.

Coalescent theory is a recent development in population genetics, which investigates the merging of gene sequences traced backward in time within gene genealogies.

The sum total of forces or systems that hold a species together. The term is used especially in the interbreeding and cohesion species concepts. Cohesion mechanisms include isolating mechanisms in sexual species as well as stabilizing ecological selection, which may cause cohesion even within asexual lineages.

Selection acting to preserve extreme phenotypes in a population. Speciation usually involves disruptive selection, because intermediates (hybrids between incipient species) are disfavored (also see Stabilizing selection).

A method of delimiting species via clustering of short stretches of DNA sequence data called “barcodes,” usually from mitochondrial DNA.

Movement of genes between populations, usually via immigration and mating of whole genotypes, but sometimes single genes may undergo horizontal gene transfer via transfection by microorganisms.

The sum total of the genetic variation within a reproductively isolated species population; this term is mostly used by supporters of the interbreeding species concept.

A synonym for genotypic cluster.

In a local area, a single genotypic cluster (or species) is recognized if there is a single group of individuals recognizable on the basis of multiple, unlinked inherited characters or genetic markers. A pair of such genotypic clusters (or species) is recognizable if the frequency distribution of genotypes is bimodal. Within each genotypic cluster in a local region, allele frequencies will conform to Hardy–Weinberg equilibrium, and the different unlinked loci will be in approximate linkage equilibrium. The presence of more than one species or genotypic cluster can then be inferred if the distribution of genotypes is bimodal or multimodal, and strong heterozygote deficits and linkage disequilibria are evident between the clusters.

The sum total of all types of factors that prevent gene flow between species, including premating mechanisms (mate choice), and postmating mechanisms (hybrid sterility and inviability). Modern authors deny that these mechanisms have necessarily evolved to preserve the species' integrity as originally assumed, though this may sometimes be the case in reinforcement of premating isolation. Isolating mechanisms are a subset of the factors that cause cohesion of species under the interbreeding and cohesion species concepts.

A grouping that contains all the descendants of a particular node in a phylogeny. Monophyly is the state of such groupings. Compare paraphyletic and polyphyletic. Butterflies (Rhopalocera) and birds (Aves) are the examples of two groups thought to be monophyletic.

A grouping that contains some, but not all, of the descendants of a particular node in a phylogeny. Paraphyly is the state of such groupings. Compare monophyletic and polyphyletic. Moths (Lepidoptera, excluding butterflies) and reptiles (amniotes, excluding birds and mammals) are examples of two groups thought to be paraphyletic.

A classification or grouping based purely on overall similarity. Pheneticists use matrices of overall similarity rather than parsimony to construct a “phenogram” as an estimate of the phylogeny. Examples of phenetic methods of estimation include unweighted pair group analysis (UPGMA) and neighbor joining. Cladists reject phenetic classifications on the grounds that they may result in paraphyletic or polyphyletic groupings.

Pertaining to the true (i.e., evolutionary) pattern of relationship, usually expressed in the form of a binary branching tree, or phylogeny. If hybridization produces new lineages, as is common in many plants and some animals, the phylogeny is said to be reticulate. Phylogenies may be estimated using phenetics, parsimony (cladistics), or methods based on statistical likelihood.

Groupings that contain taxa with more than one ancestor. “Polyphyly” is the state of such groupings. Compare paraphyletic and monophyletic. “Winged vertebrates” (including birds and bats) are examples of a polyphyletic group.

Two tricky words found frequently in the species concept debate. Reality is typically used to support one's own species concept, as in: “The conclusions set forth above … lead to a belief in the reality of species” (Poulton, 1904); similar examples can be found in the writings of Dobzhansky, Mayr, and many phylogenetic systematists. The term reality in this sense is similar to an Aristotelian essence, a hypothetical pure, albeit obscure, truth that underlies the messy actuality; unfortunately, in everyday language real also means actual (curiously, a reality in the first sense may be unreal under the second!). By rejecting the reality of species, one can therefore send very mixed messages: some readers will understand the author to be a nominalist who merely believes useful terms require no theoretical underpinning; others assume the author is nonsensically using some definition that does not apply to the actual organisms. Here, when the author discusses the reality underlying a species concept, he means it in the first sense, a hypothesis. Many authors of species concepts and some philosophers of science argue that definitions must be underpinned by a theoretical justification or reality. Other philosophers such as Wittgenstein and Popper agree that terms need no such definition to be useful.

A pair of closely related, morphologically similar species (usually sister species).

The evolutionary process of the origin of a new species.

Fertilization and mate recognition systems in the recognition concept of species, the factors leading to premating compatibility within a species. Also see cohesion, which is similar to SMRS, but includes postmating compatibility as well.

Selection which favors intermediate phenotypes.

The process whereby the numbers of species in the checklist of a group increases due to a change in species concept rather than due to new discoveries of previously unknown taxa.

III. Predictive Classifications

Cladistic hypotheses are most succinctly expressed in graphic form as branching diagrams known as clado-grams (also phylogenetic trees, trees, phylograms, or dedrograms, sometimes with special meanings). Species or the least inclusive higher taxa included in an analysis are plotted as terms (terminals) at the tips of the finest branches of the tree structure. They are grouped together by the observed pattern of distribution of shared-derived similarities or synapomorphies. Synapomorphies, or shared apomorphies, represent evolutionary novelties. Such novelties are heritable characters, and as such are constantly distributed within the terminals defined by them, whether species or higher taxa. Attributes that vary within a terminal, in contrast, are termed traits even at higher levels. Characters are shared by all members of a taxon, either in their original (ancestral) condition or in a subsequently modified form, the modern interpretation of character formalized by Norman Platnick in 1979. Synapomorphies may occur once on a cladogram or more often if the overall parsimonious distribution of characters suggests multiple origins (convergence), losses, or losses plus regains (reversals).

Hennig defined monophyletic groups as those including a common ancestral species and all of its descendant species. The goal of a phylogenetic classification is to make all groups monophyletic. Although monophyletic groups had long been recognized, Hennig's method was the first to require monophyly. Synapomorphies are taken as evidence of monophyly. Symplesiomorphy or shared primitive similarity erroneously leads to groups that include ancestral species and some but not all of its descendant species; these groups are known as paraphyletic. Errors are sometimes made while interpreting characters, and states are mistakenly grouped together as the same that have actually arisen from independent evolutionary events. Such instances of convergent evolution, parallelism, or reversal to ancestral character states are known as homoplasy. When groups are based on shared homoplasy, they include distantly related species that do not share a most recent common ancestor and are known as polyphyletic. Figure 5 shows examples of such groups referring to a primitively flightless silverfish, a damselfly, a beetle, and a fly. The best available insect classification suggests that fly + beetle constitutes one monophyletic group whose sister group is the damselfly. The silverfish is then sister to the other three combined. Were the silverfish and damselfly grouped together based on their comparatively simple metamorphosis (lacking a pupal stage), they would be paraphyletic because simple metamorphosis is a shared, primitive similarity in comparison to holometaboly. Were the small, aristate antennae of the damselfly and fly taken as similarity, the group might be described as polyphyletic since it is based on convergent similarity and not on common ancestry. This example was used for simplicity. In practice, paraphyletic and polyphyletic groups involve a much broader scale of grouping errors.

Hennig was concerned specifically with historical patterns above the level of species, and the concepts described previously pertain to how species are grouped together into higher taxa and clades. Such ideas, of course, presuppose that there is some agreement with regard to the definition of species.

Since the rise of modern genetic theory, biology in general has focused on the mechanistic aspects of species formation, basically asking “Why do species exist?” and “How do species originate and maintain their uniqueness?” Although the importance of such questions is obvious, another equally important and even more fundamental question was sometimes neglected: “What are species?” This “what” question differs fundamentally from the aforementioned questions in that it asks about a pattern rather than a process. This question, usually framed in terms of competing species concepts, was traditionally and is still logically within the purview of taxonomy. The answer to this question has direct and significant bearing on answers to related “why” and “how” questions.

The most elementary questions about biodiversity (How many species are there in a particular clade, place, or ecosystem?) require a scientific concept of species, as do successful strategies, policies, and laws to protect biological diversity. Because taxonomists are primarily concerned with the discovery, description, naming, and classification of species, they have traditionally provided the answer to the “what” question. More literature has probably been devoted to species and speciation than to any other single topic in biology, but species concepts remain highly contentious. Given so much attention, one might expect that the species “problem” is solved. On the contrary, there are more species concepts vying for adoption today than there were a century ago, and the debate among competing concepts rages on. Even if biologists could agree on one concept of species, it would remain true that we have only begun the process of exploring the species of Earth. Estimates of the total number of species living today vary tremendously from a few million to as many as 100 million. Although our ignorance about biodiversity is due largely to inadequate support for taxonomists to discover and describe the world's species, this work is impossible in the absence of an agreement regarding the concept of species to be applied.

Closely associated with the new synthesis was the biological species concept (BSC). The BSC was built on observations in the nineteenth century that sister species often lived in adjacent but separated areas, suggesting that allopatry was important in some way to species formation, particularly in animals. These ideas, combined with a shifting emphasis in biology to population genetic questions, made Ernst Mayr's persistent advocacy for the BSC extremely effective among zoologists. Currently, the majority of zoologists nominally accept the BSC, although the number of studies providing the kind of interbreeding information required by the concept are few. Botanists never accepted the BSC in large numbers, in part due to the incredibly diverse and complex genetic mechanisms in angiosperms and rampant polyploidy in pterydophytes.

With some level of discontent already in place, Hen-nig's writings forced a deeper consideration of species in the context of phylogenetic theory. Hennig pointed out that the BSC was at odds with evolutionary history since there were no clear breaks in the potential to interbreed among populations through geologic time. Projecting breeding patterns backwards through the geological record, there were no obvious places to demarcate one species from another. Hennig provided a fix for this dilemma and advocated a concept that in many respects resembled the BSC.

Donn Rosen noted that ancestral interbreeding, relative to extant populations, was plesiomorphic and therefore of little consequence to phylogeny; it was the loss of interbreeding that was of importance but which is indistinguishable from the absence of interbreeding. This, combined with a sincere desire to apply Hennigian theory to the species problem, led Rosen to develop an alternative species concept that attempted to apply cladistic analysis to populations. Rosen sought to ensure that species had novel status by making them equal to the smallest demonstrably autapomorphic units. Rosen's was the first concept explicitly couched in terms of phylogenetic theory, but it suffered from several problems. Ancestors were impossible to positively recognize given this concept, even though they clearly had existed. When two or more species arose from one polymorphic ancestral population, it was not clear that one or the other daughter was more or less apomorphic than the other. Also, this use of the idea of monophyly was at odds in logic and intent with Hennig's theories that dealt explicitly with supraspecific groupings. Despite these evident problems, some authors still advocate autapomorphic species.

George Gaylord Simpson developed an evolutionary species concept based on his view as a vertebrate paleontologist. His concept was revised and expanded by E. O. Wiley nearly 30 years later, bringing the arguments for evolutionary species explicitly in line with phylogenetic theory. This theory has no overt conflict with either phylogenetic theory or known evolutionary processes, but it is not clear how this concept is put into practice in an empirical sense.

About 20 years ago, a second generation of phylogenetic species concept emerged that was independent of cladistic analysis (so that it could provide the elements of phylogeny to be analyzed prior to such an analysis) and fully compatible with phylogenetic theory. Working simultaneously, two pairs of authors produced nearly identically worded versions of such a concept: Eldredge and Cracraft (1980) and Nelson and Plantick (1981). The phylogenetic species concept is very similar to the morphological concepts in broad use by taxonomists before they were set aside in favor of the BSC, but it is formulated specifically in a phylogentic framework. According to the phylogenetic species concept, a species is simply the smallest aggregation of (sexual) populations or (asexual) lineages diagnosable by a unique combination of character states.

Debate continues regarding the best alternative. This battle over species concepts is far from a mere academic exercise (Table I). Any effort to inventory or document biodiversity, to compare the biodiversity present in one habitat or geographic place versus another, and any wording in regulations aimed at natural resource management or biodiversity conservation will inevitably be described in terms of the numbers and kinds of species affected. Adopt the wrong concept, and we grossly under- or over-estimate biodiversity with potentially catastrophic effects. It is important that this debate proceed with all due haste, but it is no less important that we arrive at the correct answer and not simply an expeditious or democratically popular one. Every student of biodiversity has a responsibility to consider this question carefully and fully and has a stake in the outcome.

Table I. Alternative Species Conceptsa