The units of phylogenetic analysis. Species and speciation
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1 The units of phylogenetic analysis Premise: units should be natural units. = monophyletic: derived from single common ancestor. Individuals Populations Species: monophyletic collections of populations. Higher taxa: more inclusive monophyletic collections of populations. Most common unit is species. Collection of populations. Distinguished from other species by some kind of criterion: morphological, genetic, ecological. Two aspects: (1) definition and (2) diagnosis. Species and speciation Why important in phylogenetics? Evolutionary tree: branching points (nodes) represent speciation events. Process models to understand phylogenetic relationships invoke models of speciation. Models of speciation depend on concept of what species are. Biologists disagree about what species are. Origin of species is fundamental issue in evolutionary Origin of species is fundamental issue in evolutionary biology. Can t be resolved without agreement about what a species is. Two primary contexts: phylogenetics and evolutionary genetics. 1
2 The so-called species problem has plagued evolutionary biology since before Darwin s publication of the aptly titled Origin of Species. Many biologists think the problem is just a matter of semantics; others complain that it will not be solved until we have more empirical data. Yet, we don t seem to be able to escape discussing it and teaching seminars about it. M. Pigliucci BioEssays 25:596 Discussions of the nature of species seem to arouse passion and self-righteousness not found in most scientific debates. Each side tends to caricature the logic of its opponents, emphasizing i the obvious weaknesses and not mentioning the strengths. Furthermore, some of the issues appear to be philosophical, not scientific. it is hardly surprising that the response of many evolutionary geneticists has been to ignore (if not disparage) these discussions. R.G. Harrison In: Endless Forms,
3 The appropriately militant view that systematists need to embrace is that the responsibility for species concepts lies solely with systematists. If we continue to bow to the study of process over pattern, then our endeavors to elucidate pattern become irrelevant. Q.D. Wheeler & K.C. Nixon Cladistics 6:79 Species concepts Do species always exist in nature? If so, why? Do species sometimes exist in nature? If so, why? Fundamental question: are species real or nominal? Realist concept: nature is divided into discrete species. Basis: folk taxonomy. Ecologists seldom disagree over how many species exist at a given location. Nominalist concept: species are artificial divisions of a natural continuum. Basis: evolutionary lineages. 3
4 Species concepts Before Darwin, species were uncontroversial: Typological (essentialist) view dates from Aristotle. Formalized by Carl Linnaeus (Systema t Naturae, 1735) Mus Nat Hist Oxford Univ Darwin first to propose natural mechanisms for evolutionary transformations of species. Laid groundwork for scientific study of speciation. Ironically, Darwin was a nominalist: I look at the term species, as one arbitrarily given for the sake of convenience to a set of individuals closely resembling each other. In short, we shall have to treat species in the same manner as those naturalists treat genera, who admit that genera are merely artificial combinations made for convenience. This may not be a cheering prospect; but we shall at least be freed from the vain search for the undiscovered and undiscoverable essence of the term species. Charles Darwin, 1859 The Origin of Species 4
5 Nominalism and realism Other nominalists: J.B.S. Haldane (1956) P. Raven (1976) B.D. Mishler and M.J. Donoghue (1982) G. Nelson (1989) J. Mallet (2001) Semi-realist view common among botanists: Some species are real. Other groups less distinctive due to extensive hybridization or clonal reproduction. Species concepts Most modern biologists treat species as a fundamental natural unit. Identify research organisms at species level. Communicate by Linnaean binomial. But little consensus on what species are: How to define the species category. How to recognize and diagnose species. Irony: evolutionary biologists commonly use the term species with seamless exchange of ideas. Only when someone is questioned on what is meant by species does conflict arise. E.g.: endangered species. 5
6 Species concepts In practice, most species are recognized phenetically. Recognized by consistent differences in easily identifiable morphological characters (traits). Diagnosed by reliable characters: Possessed by all (or almost all) individuals. Not possessed by members of other species. Difficult to find characters relevant to all life stages. No reason why reliable characters should exist. Golden eagle e Bald eagle Haliaeetus leucocephalus Aquila chrysaetos The consensus view (more or less) Species are sets of populations of organisms. Species are held together (rendered cohesive) by sex and genetic compatibility. Conspecific individuals can potentially interbreed. Species are kept separate from other species to the extent that they do not fuse. Reproductively isolated from one another. Under normal conditions. Species are the largest units that participate in evolutionary yp processes (gene flow, adaptation, etc.) Genes replicate, organisms copulate, populations evolve, species speciate. All have common history + genetic cohesion. Higher taxa are groups of related species (clades). Clades have common history, but no cohesion. 6
7 Species concepts Practical problems of species recognition: If species evolve from common ancestor, expect awkward intermediate t cases. Differ on average, but with much variation. Sufficiently different to be recognized? No reliable characters for some closely related species. Geographic variation: good character in one location may be poor in another. Distinction is statistical rather than discrete. E.g., ring species : continuum rather than discrete. Species concepts Example of ring species: Ensatina salamanders of the Pacific coast. Spread south from Oregon on both sides of San Joaquin Valley. 7
8 Species concepts Another example of a ring species: Greenish Warblers of northern and central Asia. Originated in Himalayas, spread westward and eastward around Tibetan Plateau. Morphology and songs become more complex in both directions. Reproductively isolated in Siberia. West Siberian species East Siberian species Species concepts Controversy arises from conflict between: (1) Intuitive classification of organisms ( kinds ). Similar taxonomies produced by different cultures. (2) Continuous and complex process of evolution. No definition can neatly classify populations at every stage of development. Why should expect distinct species rather than continuous intergradation of interbreeding organisms? What kinds of genetic differences distinguish species? Species concepts influenced by causes of divergence: Selection. Drift, inbreeding (neutral theory). Founder effect and chromosomal speciation. 8
9 Species concepts Currently many formal definitions of species: Agamospecies concept Internodal species concept Biological species concept Morphological species concept Cladistic species concept Non-dimensional species concept Cohesion species concept Phenetic species concept Composite species concept Diagnosable phylogenetic species conc Ecological species concept Monophyly phylogenetic species concep Evolutionary significant unit General phylogenetic species concept Evolutionary species concept Polythetic species concept Genealogical concordance conceprecognition species concept Genetic species concept Reproductive competition concept Genotypic cluster concept Successional species concept Hennigian species concept Taxonomic species concept Mayden,
10 Species concepts Some species concepts define species at the present: a single point in time. (1) Phenetic species concept: overall similarity. (2) Biological i l species concept: interbreeding. (3) Genetic species concept: genetic isolation. (4) Recognition species concept: recognition of conspecifics. (5) Ecological species concept: selection maintains variation in forms we recognize as species. Some concepts aim to define which individuals are members of a species across time. (6) Phylogenetic and (7) evolutionary species concepts. Species concepts (1) Phenetic species concept: Based on idea that species concept shouldn t be tied to any particular evolutionary model. Informally: species is a set of organisms that: Resemble one another in terms of overall similarity. Are distinct from other species. Formally: Would specify some exact degree of phenetic similarity. Similarity is measured by a phenetic distance statistic. E.g., g, a species is a set of organisms: not more than x phenetic distance units apart. Separated by a phenetic distance of at least y units from the nearest distinct set. 10
11 Phenetic species concept In practice, phenetic concept uses as many characters as possible. Recognizes phenetic clusters using multivariate statistics. Species consist of smaller clusters that match level of similarity typical of what would have been called a species before numerical techniques became available. Species recognized on basis of suites of characters. Diagnostic characters are proxies for underlying multivariate descriptions. Distance 0 Phenetic species concept Simple extension of way species are recognized in practice. Nature contains groups of organisms that are similar phenetically. Our perceptual systems operate a cluster algorithm. Different observers tend to agree on pattern of similarity in most cases. Extensible to higher taxa (genera, families, etc.). Modern form of typological species concept? 11
12 Phenetic species concept Criticisms: Lacks sound philosophical basis. Underlying theoretical concept corresponding to a phenetic cluster? Forced to make subjective and arbitrary decisions. No unique measure of phenetic similarity or distance. Different criteria can divide organisms into different sets of groups. No criterion on which to fall back in ambiguous cases. No reason to suppose that a real pattern of morphological types exists in nature. No variants in a population are more typical or real than others. Species concepts (2) Biological species concept (BSC): defines species in terms of interbreeding. Mayr: Species are groups of interbreeding natural populations that are reproductively isolated from other such groups. Most widely accepted species concept. Predates Darwin: John Ray (17 th century). Strongly advocated by founders of modern synthesis: Dobzhansky, Mayr, Huxley. Places species within conceptual scheme of population genetics. Gene pool: abstract conception of set of interbreeding organisms, within which gene frequencies can change. Species are (possibly subdivided) gene pools. 12
13 Biological species concept BSC explains why members of species: (1) resemble one another, (2) differ from other species. Shared gene pool gives species its genetic and phenetic identity. Genes of organisms constantly reshuffled within gene pool. Family lineages (parent, offspring, etc.) blurred by gene transfer. Cohesiveness: selection favors sets of genes that interact well with other genes to produce adapted organisms. Genes not (usually) shared with other species. Biological species concept Taxonomists usually identify species by morphology, not reproduction. Morphological characters shared between individuals are indicators of interbreeding. Seek morphological criteria that mimic the interbreeding principle. Individuals of a species not morphologically uniform: Polytypic. Different species have different degrees of morphological variation. 13
14 Reproductive isolating mechanisms Emphasis on reproductive isolating mechanisms (RIMs): Any property of two species that prohibits or reduces the frequency of hybridization. Selected for by heterozygote disadvantage. Actual cases typically involve mix of several factors. Often classified into premating and postmating: (1) Premating or prezygotic mechanisms: prevent formation of hybrid zygotes. Ecological / habitat isolation: occur in different habitats in same general region (sympatric but allotopic). Seasonal / temporal: mating or flowering occurs at different seasons. Sexual / ethological: mutual attraction between sexes of different species is weak or absent. Reproductive isolating mechanisms (2) Postmating or zygotic isolating mechanisms: reduce viability or fertility of hybrid zygotes. Hybrid inviability: hybrid zygotes have reduced viability or are inviable. Hybrid sterility: F 1 hybrids of one or both sexes fail to produce functional gametes. Hybrid breakdown: F 2 or backcross hybrids have reduced viability or fertility. 14
15 Species concepts (3) Genetic species concept: Baker & Bradley (2006): We define a genetic species as a group of genetically compatible interbreeding natural populations that is genetically isolated from other such groups. Focus on genetic isolation rather than reproductive isolation: Can often be established with genetic data. Removes burden of demonstrating reproductive isolating mechanisms. Based on population-genetics theory: Bateson Dobzhansky Muller (BDM) model. Allows for understanding and prediction of genetic diversity and speciation. Species concepts (4) Recognition species concept: H.E.H. Patterson: species defined as a set of organisms with a common method of recognizing mates. SMRS: specific mate recognition system. In practice, defines species similar or identical to the biological species concept. Two versions of general reproductive species concept : key concept is interbreeding. Isolating mechanisms: prevent interbreeding between species. Recognition mechanisms: ensure interbreeding within species. 15
16 Recognition species concept Defining species by shared mate recognition has advantages: May represent more accurately what happens when new species originates: Crucial event may be evolution of new SMRS. Evolution of new isolating mechanisms might not be important; might be incidental by-products of divergence. And disadvantages: SMRS S can t be observed ed in dead specimens. e s Interbreeding more difficult to observe, usually inferred indirectly. Species concepts (5) Ecological species concept: A species is a set of organisms exploiting a single niche. Become different species when migrate among environmental resources that exist in discrete forms. Forms and behavior of organisms are adapted to resources exploited and habitats occupied. Ecological niche: set of resources and habitats exploited by members of a species. Populations form discrete phenetic clusters produced d by ecological and evolutionary processes controlling division of resources. Based on theory of evolutionary ecology. 16
17 Ecological species concept E.g.: parasites evolve appropriate adaptations to penetrate different hosts. Concept supposes that ecological niches in nature occupy discrete zones : Adaptive zone: abstract space, set by resources and competitors in nature, within which a type of body plan is adaptive. Concept originally invented by G.G. Simpson for larger categories of species (e.g., Mammalia), based on Wright s adaptive landscape. Hybrids fall between zones and are maladaptive. Hierarchy of zones corresponding to successive taxonomic levels. Evolutionary and phylogenetic species concepts Reproductive and ecological concepts aim to define how and explain why individuals should be grouped into species at one instant in time. Horizontal species concepts. Other concepts needed to include all members of species throughout its existence. Vertical species concepts. Might or might not include horizontal concepts. 17
18 Cladistic and phylogenetic species concepts (6) Cladistic species concept: Hennig: Species is a set of organisms in a lineage between two branch points. A B C (7) Evolutionary species concept: Simpson: Species is a lineage (an ancestraldescendant sequence of populations) evolving separately from others and with its own unitary evolutionary role and tendencies. Closest to the ecological concept, with added time dimension. Cladistic and phylogenetic species concepts Both concepts based on information about: Occurrence in fossil record. Phylogenetic relationships. Ancestral species (though observed later in fossil record) Same species (though observed at different times in fossil record) Different species (though possibly identical in form) 18
19 Species concepts as models Different species concepts are different models: Species concepts are simplifications aimed at understanding and prediction. Differ in assumptions about what s important/unimportant and relevant/irrelevant. Neither wrong nor right, just more or less useful. Characteristics associated with species Categories of species concepts (Pigliucci, 2003) Species concepts as models Species concept, as a model, should be useful for some purpose. Different concepts serve different purposes. Possible goals: define species so as to Correspond to discrete groups that we see in nature. Help to classify groups in a systematic manner. Help to understand how groups arise in nature. Represent evolutionary history of groups of organisms. Apply to the largest possible number of organisms. Etc. No species concept can accomplish all of these goals. Identify the nature of one s species problem, then choose concept best at solving that problem. 19
20 Species concepts as models In particular, no concept can serve needs of both evolutionary geneticists and systematists. Systematists: Fixed character-state differences between species. Inferences about phylogenetic relationships among predefined terminal taxa. Evolutionary geneticists: Variation with species. Patterns of reticulation (mating). Processes by which one lineage splits into two. The essence of the species problem is the fact that, while many different authorities have very different ideas of what species are, there is no set of experiments or observations that can be imagined that can resolve which of these views is the right one. This being so, the species problem is not a scientific problem at all, merely one about choosing and consistently applying a convention about how we use a word. J. Brookfield Genet. Res. 79:
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