BIOL2007 - BIODIVERSITY AND SPECIES 2) The biological species concept Species defined by interbreeding (Poulton 1903,

Dobzhansky 1937, Mayr 1942). Next lecture: speciation. Gene flow within each species Today: (1) nature of species no hybridization or gene flow betwen species (2) whether this indicates speciation differs from Lack of gene flow due to isolating mechanisms microevolution. (Not necessarily "mechanisms" in any sense, I prefer the • What are species? term "reproductive isolation") • How do species differ from each other? • How many species are there? We will briefly Types of reproductive isolation cover species-level biodiversity. A) Pre-mating isolation {or pre-zygotic isolation} a) Ecological/seasonal isolation - mates do not meet Species "concepts" - What are species? b) Behavioural isolation - meet but do not attempt mating Darwin proved species evolved c) Mechanical isolation - attempts at mating do not work! But a difficulty: B) Post-mating {or post-zygotic} isolation Species weren’t created kinds, with an essence. They d) Gametic incompatibility - gametes die before gradually evolved from each other. fertilization (note: post-mating but pre-zygotic) So where is the dividing line? A pragmatic solution: e) Hybrid inviability – hybrid zygotes have reduced fitness: Darwin’s view of species -- species differ from races • genomic factors and morphs via gaps. e.g. Primula (primrose, oxslip, • hybrids are not suited ecologically and cowslip), and human races. • reduced mating propensity. f) Hybrid sterility though may survive & mate as normal).

g) Sexual selection against hybrids.

Species 1 Problems with the biological species concept head a) Does not apply in allopatry. Species become less Species 2 clear over large spans of space (in geography) or time width (in the fossil record). b) Natural hybridisation/introgression occurs.

10-12% of bird and butterfly species, 6% of mammal

spp. hybridise naturally. (Hybrid fraction < 1/1000 in body size populations). Introgression common. Examples: ducks, mammals e.g. blue whale x fin whale,

the world’s biggest animal, plants (> 20% of species. Species concepts Hybridization and introgression are important topics in Today: much debate, many "species concepts". conservation and agriculture. 1) Morphological species concept. Species delimited by gaps in morphology. 3) Ecological species concept e.g. (i) Darwin: Primula veris (primrose) and Primula Leigh Van Valen (1970s) species concept based on elatior (cowslip) are varieties of the same species -- ecological niche. many intermediates or hybrids are found. (ii) Similarly, Adaptive radiations: species evolve to occupy multiple races of humans: same species. ecological niches, especially on islands. Similar In neither case is it easy to find a dividing line. processes undoubtedly occur on the world's major

mainlands as well. e.g. the radiation of mammals in the In 1960s-1970s, phenetic species concept. A Tertiary (64 million years ago), after the demise of the multivariate statistical version of Darwin’s ideas. dinosaurs.

However some problems with phenetic concept: Problems a) Morphological gaps within species. a) Sibling species may have same niches. (Eventually: e.g. Peppered moth or Papilio memnon morphs. loss of one species via competition?) b) Ecological morphs within species. Adaptations often b) Lack of morphological differences between species: differ in different parts of a species’ range (see Evolution There are often sibling species which are in space and time). (i) morphologically similar, though differ genetically. The cichlid fish Cichlasoma from Cuatro Cienagas, (ii) evolve more or less separately Mexico, has multiple morphs that do different things: (iii) little or no hybridisation/gene flow: bottom living mollusc-feeder: grinding teeth • willow warbler & chiff-chaff: sing different songs pelagic piscivore: sharp teeth • Drosophila fruitflies: D. pseudoobscura and D. algae/detritivore: rounded teeth persimilis differ chromosomally So hard to say ecology is the definition of species. • Anopheles mosquitoes: differ in habitat, biting preference, and malaria-carrying

1 4) Cladistic and phylogenetic species concepts Genetics and the definition of species Cladistic movement founded by Willi Hennig in the Let’s update Darwin’s view of species with Mendelian 1950s. If higher taxa are defined by means of genetics ideas of gene flow (which Darwin did not have). phylogeny, then so should species, reasoned cladists. Species 1 Species 1 (mate recognition) gene flow, pre-mating hybridization isolation

Species 2 Species 2

disruptive or divergent Outgroup selection = post-mating isolation

Species are genetically differentiated populations potentially connected by gene flow. Gene flow may be very low (as in the biological species Thus: phylogenetic (based on monophyly) and concept), or in geographic isolation. diagnostic species concepts (based on diagnostic Or: if much gene flow; collapse to a single species. characters, such as morphology or mtDNA bases). Species are then clusters of genotypes with Unfortunately, there are Problems: discontinuities or gaps separating them. a) Apparent phylogenies are hypotheses, not Gene flow (weak pre-mating isolation) might break down necessarily real groups. For example, mtDNA may genetic differences. Therefore: Gene flow, if it exists, evolve differently from nuclear genes. So unstable must be balanced by disruptive selection -- intrinsic definitions result. (post-mating isolating mechanisms) or extrinsic (as in b) Many isolated populations may be monophyletic; but ecological concept). their evolution does not alter their mainland ancestor in Biological and ecological species concepts are any way. Cladistic concepts → many spp., only faintly explanations of the existence of distinct groups. recognizable. Species become more phylogenetically “real” c) Hybridization between branches of a phylogeny. A (monophyletic) as they emerge from cross-linking phylogeny is really a mass of "genealogies" at different caused by hybridization. (But never absolute?). loci. So is average phylogeny (sometimes called a "consensus" phylogeny) the "true" species phylogeny? Genetic differences between species Not exactly! Studying actual data more fruitful than philosophy. Many alternative evolutionary and phylogenetic species Species differ in ways similar to different races or concepts which attempt to answer these problems. None geographic populations (see previous lecture), only are (yet) clearly accepted. more. Some of the ways in which species differ:

5) Rank-free taxonomy, and giving up on species a) Morphological differences (Darwin’s definition, altogether! Do away with species altogether? But then above). Morphology differs between races and how would we communicate about groups of organisms. populations as well; as already mentioned. My own view: species will remain a convenient naming device to classify animals and plants. b) Genome-level differences. Francisco Ayala’s surveys There must be a certain validity to species, or bird or with enzyme loci on Drosophila. Differences: species > plant guides wouldn't be very useful. sibling species > races. But we shouldn’t take the "reality" of species too seriously. c) Chromosomal differences. For example: humans and chimpanzees (see Chromosomal Evolution) common in Why are there so many species concepts? many spp. What should practising evolutionary geneticists like you Again many subspecies and races also differ do, faced with such a diversity of opinion? chromosomally, only somewhat less. Evolutionary biologists, often think biological species Polyploidy is an exception to gradual differences. concept is best. Common feature of plant species differences. offspring Many taxonomists and systematists prefer some form of of diploid (2N) x tetraploid (4N) crosses are triploids phylogenetic species concept (3N), usually completely sterile. Ecologists often use the ecological species concept. People are partisan to their own expertise! d) Signals used in mating. Sexually-selected colours, tail Which do you prefer? length in birds, pheromones in moths, other insects, and even mammals are all involved in species recognition as well.

2 Crickets and grasshoppers, as well as frogs, species- Biodiversity specific sounds are required; fireflies, recognize each The sum total of diversity at all levels of the evolutionary other by means of coded flashes. hierarchy Again, these differences easily derived from mate choice • genetic diversity within populations differences within species. • genetic diversity between populations & races • diversity of species e) Hybrid inviability and sterility - genomic • … of genera incompatibility. Mules (donkey x horse hybrids, which • … of ecosystems, biomes etc. are sterile); chromosomal heterozygotes. The species traditionally viewed as most important. However, other species seem to have no hybrid see E.O. Wilson’s The diversity of life (1992) problems: Darwin’s finches, ducks Once again, species differ from races only in degree of Species diversity hybrid inviability and sterility, not in kind. Most of diversity is not mammalian, or even vertebrate. Beetles make up 20% of all described species! Hybrid breakdown: F1 hybrid between two species may Insects in general: 53% of described species. be alright, but backcrosses or F2 crosses produce inviability or sterility. Caused by recessive epistatic Total described species 1,413,000 genes becoming homozygous during these crosses. Animals 1,032,000 Genes causing incompatibility must be epistatic; can you Insects 751,000 see why? Beetles 290,000 Special case of hybrid inviability/sterility: Haldane's Plants and fungi 350,000 Rule: “When one sex of F1 hybrid between species is inviabile or sterile, that sex is usually the heterogametic Bias of using described species sex,” rather than the homogametic sex. Works in 1) Entomologists (Terry Erwin and others): • mammals, Drosophila (XY , XX ), also in birds, Fogged canopies of South American tree species butterflies (ZZ , WZ ). Probably due to recessive • Counted unidentified, host-specific beetles effects of genes causing incompatibility on the X. • Calculated may be as much as a 30x more species than currently described. f) Genealogical differences. Humans and chimps • 30,000,000 is their estimate. mutually monophyletic at many loci, but not MHC. 2) Bacteriologists: Heliconius cydno and H. melpomene: • Prokaryotic world is far more diverse DNA • g) Ecological differences. Maybe more diverse in “species” • For example: adaptive radiations on islands. Darwin’s Mostly not discovered (e.g. recent discoveries of finches are well-known. “extremophiles” in deep sea vents, in granite) Hawaiian honeycreepers are even more extraordinary. Genetic diversity (and metabolic diversity) therefore Finch-like ancestors → nectarivores, insectivores, gives a different view to species diversity: most of the frugivores, + seed-eating forms. genetic diversity is in the prokaryotes. But once again: no clear dividing line between races and species in the degree of ecological differentiation (see FURTHER READING ecological species concept). FUTUYMA, DJ 2005. Evolutionary Biology. Chapter 15

(pp. 353-378). Species. Genetic differences between species FREEMAN & HERRON 2001. Chapter 12 (or equivalent • multiple loci in 2004 edition) • species more different than geographic races WILSON, EO 1992. The diversity of life. • but not qualitatively more different Most parsimonious (simplest)explanation: usual Next time: how does all this diversity evolve? The study microevolutionary forces - selection, drift, mutation - of speciation. explain speciation.

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