This week we are having our first discussion about speciation with gene flow. Our topic this week is hybridization.  Readings are below and after the fold.

Required readings for Week 4:
Blair, W. F. 1951. Interbreeding of natural populations of vertebrates. The American Naturalist 85:9–30. [jstor link]

Stebbins, G. L. 1959. The role of hybridization in evolution. Proceedings of the American Philosophical Society 103:231–251. [jstor link]

Harrison, R. G. 1986. Pattern and process in a narrow hybrid zone. Heredity 56:337–349. [doi link]

Rieseberg, L. H., C. Van Fossen, and A. M. Desrochers. 1995. Hybrid speciation accompanied by genomic reorganization in wild sunflowers. Nature 375:313–316. [doi link] Continue reading →

Alan Templeton, Hamp Carson, Brian Charlesworth, and Nick Barton

By the early 1940s the importance of geographic isolation to speciation had been firmly established, and few have denied its important role since.  Although the geographic distributions of closely-related organisms rather clearly pointed to an important role for geographic isolation in speciation, it was not immediately clear from these distributional patterns what actually caused speciation.  Mayr and other architects of the synthesis discussed a wide range of hypothesizes mechanisms of speciation in the 1930s and 40s.

In 1954, however, Mayr began to advocate a mechanism for allopatric speciation that would strongly influence decades of subsequent work on speciation.  Marshaling evidence from nature – and from southeast Asian birds in particular – Mayr shows that widespread species on large islands are often relatively invariant while related populations isolated on smaller peripheral islands often exhibit extraordinary levels of phenotypic divergence.  To explain this pattern, Mayr developed a model for speciation involving isolation of small peripherally isolated populations that was inspired by population genetic studies of Fisher, Wright, Dobzhansky, and others.  In formulating this model, Mayr introduced several concepts that would strongly influence subsequent work on speciation, including the “co-adapted gene complex” and the idea that speciation tends to involve “genetic revolutions.”  Genetic revolutions involve a cascade of changes resulting from epistatic interactions among loci. Although Mayr never dismissed the important role that ecological variation and natural selection might play during founder events, he did argue that genetic revolutions in isolated populations are more important than selective differences experienced by populations connected by gene flow.

After Mayr proposed his admittedly “speculative” model involving genetic revolutions in peripherally isolated populations (later termed “peripatric speciation” [Mayr 1982]) several decades would pass before population geneticists developed more elaborate models to account for speciation resulting from genetic revolutions in founder populations.  In the late 1960s and early 1970s, the geneticist Hampton “Hamp” Carson developed his influential model of founder-flush speciation based on work with Hawaiian Drosophila.  Carson agreed with Mayr that adaptation via natural selection within a single geographically widespread population was insufficient for speciation, and that speciation was more likely accomplished by “a series of catastrophic, stochastic genetic events” that occur when small founder populations invade new territory.

Carson offered a very different explanation from Mayr’s to explain divergence of founder populations.  Most importantly, rejected Mayr’s assertion that founder populations diverge due to a dramatic reduction in genetic diversity; instead, Carson believed that founder populations tend to maintain rather high levels of genetic variation.  To Carson, however, this variation existed in the ancestral population as part of a “closed genetic system” that was not readily altered by selection or recombination under normal conditions because it was tied up in co-adapted gene complexes that were not readily altered without significant negative fitness consequences.  However, when selection was relaxed during a period of dramatic population growth associated with colonization of a new region – the flush period – recombination could break up coadapted gene complexes belonging to a species’ closed genetic variability system.  Although Carson viewed this release of genetic variation in a closed system as largely stochastic, his model was less reliant on genetic drift than Mayr’s because he believed that once variation was released it could in fact be very responsive to natural selection.   Influenced by Carson’s work, Templeton would later develop even more elaborate theories involving so-called genetic transilience.  By the mid-1980s these theories had gained considerable popularity and even played a central role in development of Eldgredge and Gould’s controversial theory of punctuated equilibrium.

By the early 1980s criticisms of founder event speciation via genetic revolution where emerging, led by papers by Charlesworth, Barton, Lande and others.(Charlesworth and Smith 1982, Charlesworth et al. 1982, Barton and Charlesworth 1984)  These papers ushered in the modern era of work on the genetics of speciation and resulted in an exchange between those who favored genetic revolutions and founder event speciation and those who favored gradual evolution of reproductive isolation in the pages of the Annual Review of Ecology and Evolutionary Biology (Barton and Charlesworth 1984, Carson and Templeton 1984).  The opponents of founder event speciation via founder-flush and transilience focused attention on core principles of population genetics and the lack of evidence for the type of genetic revolutions originally advanced by Mayr and later expanded and revised by Carson and Templeton.

This debate hardly marked the end of the controversy, which continued in the literature for more than a decade after this original exchange (Slatkin 1996, 1997, Charlesworth 1997, Gavrilets and Hasting 1996, Rundle et al. 1998, 1999, Templeton 1999).  Although founder events models are no longer widely discussed by population geneticists, Templeton remains a dedicated advocate for the role of founder events and transilience in speciation (Templeton 2008).

Readings are after the fold. Continue reading →

Jordan and Cracraft.

Geographic isolation is widely recognized as one of the most important factors that contributes to the formation of new species.  As with many ideas in evolution, however, support for geographic isolation has vacillated over time, due to a variety of factors that include Darwin’s shifting views on the role of isolation (Sulloway 1979), the emergence of alternative theories involving macromutation in the early 20th century (Allen 1969), and persistent fascination with sympatric speciation.

Our first reading for this week is from David Starr Jordan (1851-1931), an early and influential advocate for the importance of geographic isolation to speciation (Jordan 1905, 1908).  Trained as a botanist and ichthyologist, Jordan is known more broadly as a peace activist, president of Indiana University (at the age of 34), and founding president of Stanford University.  Jordan (1905) used examples from nature compiled both by himself and other prominent biologists of the time (e.g., Stejneger, Grinnell, Merriam, Gilbert) to show that most closely related species or subspecies tend to occur geographically adjacent to one, rather than sympatrically, a pattern he interpreted as evidence for the importance of geographic isolation to speciation.  Included among his many examples, are marine organisms on either side of the Isthmus of Panama, which Jordan believed diverged when the Isthmus arose during the Miocene¹.

It is important to view Jordan’s forceful advocacy for the importance of geographic isolation within the broader context of evolutionary thought in the early 20th century.  During this period, which was subsequently recognized as “the eclipse of Darwinism,” non-Darwinian theories of evolution – including Hugo De Vries’s mutation theory and Henry Fairfield Osborn’s advocacy for the neo-Lamarckian principle of Orthogenesis – were attracting considerable attention (Allen 1969).  A supporter of Darwinian theory, Jordan used his paper to argue against these alternatives, which often emphasized the importance of speciation without geographic isolation (i.e., sympatric speciation). Jordan’s 1905 paper provoked immediate debate, with critics particularly concentrated among botanists (Lloyd 1905, Abrams 1905, Leavitt 1907, Allen 1907, Jordan 1908).

Although the principle that geographic isolation was a near universal feature of speciation was once referred to as “Jordan’s Law” (Allen 1907, Michael 1913) this term didn’t catch on, and Jordan’s has since been eclipsed by Mayr as the primary advocate for geographic isolation².  Along with Dobzhansky and other architects of the Modern Synthesis, Mayr developed the “New Systematics” in the early to mid-20th century.  Mayr was the token neontological systematist among the four synthesis authors who published important monographs following a series of lectures at Columbia University in the 1930s and 40s ³. In our second reading – chapter 7 of Mayr’s 1942 monograph [pdf link] – Mayr lays the foundation for modern work on geographic isolation during speciation.  Just as Jordan did decades previously, Mayr marshals substantial evidence from nature to support allopatric speciation, often involving identification of closely related or polytypic species that occur geographically adjacent to one another. As central as Mayr’s advocacy and detailed discussion were to acceptance of the importance of allopatric speciation, the notion that geographic differentiation was important to animal speciation was already “almost universally accepted as an explanation of most speciation in animals” in the early 1940s (Smith 1942) ⁴.

Our third reading involves another major advance in the study of allopatric speciation – namely, the emergence of vicariance biogeography in the 1970s.  Vicariance biogeography used the new discipline of Hennigian systematics to diagnose speciation events tied to emergence of geologic or environmental barriers to dispersal.  The new perspective provided by vicariance were made possible in part due to a new appreciation for earth’s geologic history that stemmed from widespread acceptance of plate tectonic theory in the mid-1960s.  Early advocates of vicariance biogeography included the ichthyologist Gareth Nelson and his colleagues at the American Museum of Natural History, as well as the eccentric Venezuelan biogeographer Léon Croizat (Nelson 1973, Croizat et al. 1974, Nelson 1974, Platnick and Nelson 1978).  These early vicariance biogeographers drew a clear distinct between the ad hoc explanations of previous biogeographers that tended to focus on dispersal and the testable predictions of vicariance.  Our reading on vicariance is an early classic by the AMNH ornithologist Joel Cracraft (1982).

Although the approaches introduced by vicariant biogeographers for investigating the impact of historical geologic events on the distribution of species are still used today, attention on the role of geographic isolation during speciation shifted during the early 1990s to focus on intra-specific analyses, a field that would become known as “phylogeography” (Avise 2000).  This emphasis on patterns of differentiation within species was, in many ways, a return to the population level approach advocated by Mayr and others during the Synthesis.   Based largely on analyses of animal mitochondrial DNA, phylogeography quickly grew into a major discipline in evolutionary biology and systematics, and dominated work on geographic differentiation in nature throughout much of the 90s and early 00s.  The american geneticist and ecologist John Avise, who pioneered the use of mtDNA as a marker to diagnose geographic genetic differentiation in nature, is widely regarded as the father of phylogeography (Avise 2000).  Our reading this week is a classic paper by Bermingham and Avise (1986) on comparative phylogeography of fishes from the southeastern United States.

Footnotes:
¹ Interest in the role of the Isthmus of Panama in marine speciation was reinvigorated by studies by Nancy Knowlton and others who used molecular genetic techniques to investigate this pattern and its timing (Knowlton et al. 1993, Knowlton 1993, Knowlton and Weigt 1998).

² Jordan would distance himself from credit for advocating the importance of geographic isolation, arguing in 1908 that Moritz Wagner was “master” of this idea (Jordan 1908). It should be noted, however, that his desire to credit Wagner with this idea did not deter him from using the term “Jordan’s Law” repeatedly in this 1908 contribution.

³ The other authors who published monographs after giving lectures in Columbia’s Jesup series were the paleontologist George Gaylord Simpson (Tempo and Mode in Evolution 1944), the botanist G. Ledyard Stebbins (Variation and Evolution in Plants, 1950) and the geneticist Theodosius Dobzhansky (Genetics and the Origin of Species, 1937). However, see Cain (2002) for some backstory on Dobzhansky’s “Jesup lectures.”

⁴ The author of this quote is Hobart M. Smith the famously prolific herpetologist who has authored over 1,600 publications. At the time he wrote his 1942 article on species and subspecies in rattlesnakes he was a Professor of Zoology at the University of Rochester. On September 26th, 2012 he will celebrate his 100th birthday.

More details and our list of readings are below the fold. Continue reading →