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** I expect you to read: Avise, J.C. 2004. Chapter 7: Speciation and hybridization. In Molecular Markers, Natural History and Evolution (2nd edn.). Chapman and Hall, New York.
Having at least briefly considered the problems of phylogenetics and systematics using genetic markers, we will turn to speciation. This is one of the fundamental problems of evolutionary biology -- how do new species arise? What are the patterns and processes underlying the bewildering diversity of species that we are unfortunately destroying at a rate that equals or exceeds the rate at which we uncover them? From here I will go on to population genetics.
Some history of landmarks in the study of speciation:
This is a huge subject area. Many classics exist, perhaps the most famous of which is Darwin’s Origin of Species, published in 1857. I have listed some of the classic books in a section titled "classics". Many of these, though old, are very well worth reading.
Here are the topics I will cover:
Some of the major issues:
I. Allopatric vs. sympatric speciation (+ parapatric)
Almost certainly most speciation occurs allopatrically (that is, when the forms occur in different places). The main driving forces appear to be stochastic -- drift and/or mutation (both stochastic forces) drive the divergence between the forms, although sometimes very different selection pressures (natural selection) may be the dominant force. Reduced gene flow (lack of "migration" in the population genetics sense) is also important. For example, the rise of the Andes appears to have been very important in producing patterns of genetic differentiation in neotropical plants and animals (Gascon et al., 2000). The best-worked examples of sympatric speciation in animals used to be for Rhagoletis flies (Feder et al., 1988). More recently, it has become a very active area for fish (Schliewen et al., 1994) and brood parasitic birds (Sorenson et al., 2003). A major driving force here may be specialization on different host plants or different habitats and resources (in the case of fish or birds). As the host plants diverge in phenology, secondary compounds or other ecological features, it becomes more and more disadvantageous to fall "somewhere in the middle". The eventual result may be the evolution of reproductive isolating mechanisms that reduce or prevent successful offspring production across forms. Some of the spectacular radiation of African cichlid fishes is probably also a result of sympatric speciation, perhaps driven by a combination of ecological and sexual selection (Schliewen et al. 1994; but see Meyer et al. 1996). Recent work (Verheyen et al., 1996) on the cichlids also suggests that water level lowering created separated lakes that further promoted speciation processes (i.e., more traditional allopatric speciation). One of the "fly" guys reviewed sympatric speciation in Trends in Ecology and Evolution (Bush, 1994). We will come back to an example of "ecological" sympatric speciation in a later section. Sympatric speciation can occur more readily in plants (Savolainen et al., 2006), because plants can change their chrosome number (polyploidy) and persist or spread by asexual reproduction. Parapatric speciation occurs where the ranges of two forms abut but do not overlap extensively. In such cases, lower fitness of hybrids drives increased differentiation, eventually resulting in premating isolation.
Fig. 1 Diagram of modes of speciation (from the Wikipedia page: http://en.wikipedia.org/wiki/Allopatric_speciation)
II. Sexual selection and speciation
Ever since Darwin (1871) it has been apparent that
sexual selection may be a potent force in speciation. Perhaps the most
succinct theoretical treatment of the idea is by Russ Lande (1981). Strong
selection on secondary sexual traits (ornaments such as plumes or behaviors
such as courtship displays) can lead to rapid divergence that produces
reproductive isolation. See also the work by Schluter and Price (1993).
Mary Jane West-Eberhard (1988) produced a classic treatment of sexual selection
and the intriguing additional idea of social selection. Sexual selection
produces the classic sexually dimorphic traits that distinguish, for example,
peacocks from peahens. Social selection may be equally intense but produces
monomorphic exaggerated traits. Good examples would include keel-billed
toucans (Ramphastos sulfuratus) and puffins (Fratercula spp.). In such species, both mates compete intensively for scarce resources
(e.g., nesting cavities for toucans and burrows for puffins) as well as
for access to the best mates of the opposite sex (both sexes compete for
mates and both parents invest heavily in parental care). Speciation here
was probably NOT ecological -- the two sister species (horned and Atlantic)
have different breeding microhabitats (rock crevices and earth burrows
respectively), whereas the two most different species (Atlantic and tufted)
are both burrowers. Whether the force is sexual or social selection a common
feature is a certain degree of arbitrariness (stochasticity). Toucans in
one location may become red-breasted and yellow-billed, while those elsewhere
may become yellow-breasted and green-billed. Natural selection, in contrast,
usually has a certain directionality or even optimality attached to it.
John Endler has been a proponent of the idea that traits such as plumage
color are predictable from features of the environment -- in a paper on
manakins, he and Marc Théry argued that the particular colors of
male plumage are a fine-tuned fit to the ambient light environment (Endler
and Théry, 1996). Sexual selection may not always be a diversifying
force. An interesting example of how sexual selection can help mask speciation
is provided by my graduate school colleagues Dave and Jean Zeh (1994).
They studied several different species of pseudoscorpions (Cordylochernes)
that ride on harlequin beetles. Although the pseudoscorpions have undergone
considerable genetic divergence, sexual selection has maintained a consistent
morphology across the set of different species. [See Turner and Burrows
(1995) for a model for sympatric speciation via sexual selection].
Behavior and hybrid zones: Two recent examples exist for how the dynamics of hybrid zones may be affected by the mating system, sexual selection and behavioral differences among hybridizing forms. Sievert Rohwer and his colleagues have studied the interaction between Townsend's Warblers (Dendroica townsendi) and Hermit Warblers (Dendroica occidentalis). The Townsend's males are more aggressive and the hybrid zone is moving rapidly into the range of the Hermit Warbler. Behavioral asymmetries are therefore driving Townsend's genes into Hermit country -- Hermit females mate with Townsend's males but not vice versa (Pearson and Rohwer, 2000; Rohwer and Wood, 1998). I worked on a hybrid zone between two species of manakins in Panama. The Golden-collared Manakin (Manacus vitellinus) and the White-collared Manakin (M. candei) come together in a narrow hybrid zone along the Caribbean coast of Panama near the Costa Rican border. Beyond the hybrid zone is a zone of introgression. Here the birds are genetically and morphologically indistinguishable from White-collared Manakins (Parsons et al., 1993). One trait, though, the golden collar, has crossed the species boundary. The clines for the genetic and morphological traits are narrow and coincident, but the cline for collar color is displaced 50 km to the west (Brumfield et al. 2001). Using taxidermic mount experiments, my colleagues and I were able to show that Golden-collared males are more aggressive and that the introgression zone "lemon-collared" males resemble Golden-collared males not only in their collar color but also in their behavior toward other males (McDonald et al., 2001). A recent study by Stein and Uy (2006) updates that work by demonstrating that female choice may be the most important driving force behind the advantage to the introgressive yellow plumage.
Fig. 2. Manakins (Pipridae) in the genus Chiroxiphia. Manakins have a lek mating system, with strong sexual selection on males for mating success.
Has sexual selection promoted speciation in the family?
III. Islands as "natural laboratories" for exploring speciation
We all know how much of an influence the juxtaposition of variation and similarity among islands in the Galapagos archipelago played in crystallizing Darwin’s thoughts on evolution, speciation and natural selection. Perhaps less well known is the influence of the Indonesian archipelago on Alfred Russell Wallace, whose development of ideas on evolution and speciation paralleled Darwin's. Islands have continued to play an important role in shaping the thinking of biologists on speciation. Much of Ernst Mayr’s (1942) classic work on speciation derived from his extensive knowledge of the birds of the Indonesian archipelago. A recent classic on speciation returns to the Galapagos. Peter Grant and his wife Rosemary have long studied the evolution of Galapagos finches (Grant, 1986; see particularly Chapters 10, 11, 13; Grant and Grant, 1996, 1997). Another classic example of the radiation of a group on an island is the Hawaiian honeycreepers (Lovette et al., 2001).
Fig. 3. Hawaiian honeycreepers radiated from an ancestral founder that was a cardueline finch.
Two recent studies provide interesting
insights into patterns of differentiation along the Hawaiian archipelago.
Roderick and Gillespie (1998) recently examined the patterns of speciation
in arthropods of the Hawaiian archipelago (Arthropods comprise over 75%
of the endemic biota of the Hawaiian Islands). Much of their study depended
on compiling the results of many previous studies. Their major conclusions
included: classifying patterns of speciation within Hawaiian arthropod
lineages into three categories: (i) single representatives of a lineage
throughout the islands; (ii) species radiations with either (a) single
endemic species on different volcanoes or islands, or (b) multiple species
on each volcano or island; and (iii) single widespread species within a
radiation of species that exhibits local endemism. A common pattern of
phylogeography is that of repeated colonization of new island groups, such
that lineages progress down the island chain, with the most ancestral groups
(populations or species) on the oldest islands. While great dispersal ability
and its subsequent loss are features of many of these taxa, there are a
number of mechanisms that underlie diversification. These mechanisms may
be genetic, including repeated founder events, hybridization, and sexual
selection, or ecological, including shifts in habitat and/or host affiliation.
The majority of studies that Roderick and Gillespie reviewed suggested
that natural selection is a primary force of change during the initial
diversification of taxa.
Fleischer et al. (1998) used the fact that the Hawaiian Islands are know to have arisen sequentially to put a geologically-based time window on speciation events along the archipelago. Kauai is estimated to have arisen 5.1 MYA (million years ago), compared to the big island of Hawaii at 0.43 MYA. The sequential geological pattern provides a relatively rare opportunity to calibrate the molecular clock against a well-documented pattern of geological change as well as phylogenetic trees.
Fig. 4. Map of the Hawaiian islands, showing the age-graded sequence from oldest in the NW to youngest in the SE (from Fleischer et al. 1998).
IV. Species concepts -- biological vs. phylogenetic
V. "Instant speciation" via polyploidy etc.
VI. Ecological vs. "genetic" (drift and mutation) speciation
VII. Punctuated evolution and speciation
VIII. Shifting balance theorem of Wright vs. mass selection/large size theory of Fisher
IX. Haldane's rule
In the event of hybridization, the heterogametic sex is the most likely to suffer reduced fertility (hybrid sterility) or viability. In mammals, this means male sterility (e.g., mules); in birds, females are the heterogametic sex. Haldane's rule can play an interesting, if somewhat minor role in the dynamics of speciation [See Orr, 1997; Turelli, 1998; Tegelström 1987 provides a case history for Ficedula flycatchers].
*Darwin, C. 1859. The Origin of Species by Means of Natural Selection or the Preservation of Favoured Races in the Struggle for Life. 1962 edition by Collier Books, New York.
*Darwin, C. 1871. The Descent of Man, and Selection in Relation to Sex. 1981 edition by Princeton University Press, Princeton, NJ.
*Dobzhansky, T. 1937. Genetics and the Origin of Species. Columbia University Press, NY.
Endler, J.A. 1977. Geographic Variation, Speciation and Clines. Princeton University Press, Princeton, NJ.
*Fisher, R.A. 1958. The Genetical Theory of Natural Selection. 2nd edn. Dover Press, N.Y. (1st published in 1930 by Oxford University Press).
*Gould, S.J. 1973. Ontogeny and Phylogeny. Harvard University Press, Cambridge, Mass.
*Mayr, E. 1942. Systematics and the Origin of Species. Columbia University Press, NY.
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Simpson, G.G. 1944. Tempo and Mode in Evolution. Columbia Univ. Press, NY.
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*Wright, S. 1978. Evolution and the Genetics of Populations, Vol. 4: Variability Within and Among Natural Populations. University of Chicago Press, Chicago.
Other references and literature cited:
Avise, J.C. 1994. Chapter 7: Speciation and hybridization. In Molecular Markers, Natural History and Evolution. Chapman and Hall, New York.
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