Reinforcement (speciation)

Reinforcement is a process of speciation where natural selection increases the reproductive isolation (further divided to pre-zygotic isolation and post-zygotic isolation) between two populations of species. This occurs as a result of selection acting against the production of hybrid individuals of low fitness. The idea was originally developed by Alfred Russel Wallace and is sometimes referred to as the Wallace effect. The modern concept of reinforcement originates from Theodosius Dobzhansky. He envisioned a species separated allopatrically, where during secondary contact the two populations mate, producing hybrids with lower fitness. Natural selection results from the hybrid's inability to produce viable offspring; thus members of one species who do not mate with members of the other have greater reproductive success. This favors the evolution of greater prezygotic isolation (differences in behavior or biology that inhibit formation of hybrid zygotes). Reinforcement is one of the few cases in which selection can favor an increase in prezygotic isolation, influencing the process of speciation directly. This aspect has been particularly appealing among evolutionary biologists.

The support for reinforcement has fluctuated since its inception, and terminological confusion and differences in usage over history have led to multiple meanings and complications. Various objections have been raised by evolutionary biologists as to the plausibility of its occurrence. Since the 1990s, data from theory, experiments, and nature have overcome many of the past objections, rendering reinforcement widely accepted, though its prevalence in nature remains unknown.

Numerous models have been developed to understand its operation in nature, most relying on several facets: genetics, population structures, influences of selection, and mating behaviors. Empirical support for reinforcement exists, both in the laboratory and in nature. Documented examples are found in a wide range of organisms: both vertebrates and invertebrates, fungi, and plants. The secondary contact of originally separated incipient species (the initial stage of speciation) is increasing due to human activities such as the introduction of invasive species or the modification of natural habitats. This has implications for measures of biodiversity and may become more relevant in the future.

Reinforcement has had a complex history in that its popularity among scholars has changed over time. Jerry Coyne and H. Allen Orr contend that the theory of reinforcement went through three phases of historical development:

Sometimes called the Wallace effect, reinforcement was originally proposed by Alfred Russel Wallace in 1889. His hypothesis differed markedly from the modern conception in that it focused on post-zygotic isolation, strengthened by group selection. Theodosius Dobzhansky was the first to provide a thorough description of the process in 1937, though the term itself was not coined until 1955 by W. Frank Blair. In 1930, Ronald Fisher laid out the first genetic description of the process of reinforcement in The Genetical Theory of Natural Selection, and in 1965 and 1970 the first computer simulations were run to test for its plausibility. Later population genetic and quantitative genetic studies were conducted showing that completely unfit hybrids lead unequivocally to an increase in prezygotic isolation.

Dobzhansky's idea gained significant support; he suggested that it illustrated the final step in speciation, for example after an allopatric population comes into secondary contact. In the 1980s, many evolutionary biologists began to doubt the plausibility of the idea, based not on empirical evidence, but largely on the growth of theory that deemed it an unlikely mechanism of reproductive isolation. A number of theoretical objections arose at the time and are addressed in the Arguments against reinforcement section below.

By the early 1990s, reinforcement saw a revival in popularity among evolutionary biologists; due primarily from a sudden increase in data—empirical evidence from studies in labs and largely by examples found in nature. Further, computer simulations of the genetics and migration patterns of populations found, "something looking like reinforcement". The most recent theoretical work on speciation has come from several studies (notably from Liou and Price, Kelly and Noor, and Kirkpatrick and Servedio) using highly complex computer simulations; all of which came to similar conclusions: that reinforcement is plausible under several conditions, and in many cases, is easier than previously thought.

Confusion exists around the meaning of the term reinforcement. It was first used to describe the observed mating call differences in Gastrophryne frogs within a secondary contact hybrid zone. The term secondary contact has also been used to describe reinforcement in the context of an allopatrically separated population experiencing contact after the loss of a geographic barrier. The Wallace effect is similar to reinforcement, but is rarely used. Roger Butlin demarcated incomplete post-zygotic isolation from complete isolation, referring to incomplete isolation as reinforcement and completely isolated populations as experiencing reproductive character displacement. Daniel J. Howard considered reproductive character displacement to represent either assortive mating or the divergence of traits for mate recognition (specifically between sympatric populations). Reinforcement, under his definition, included prezygotic divergence and complete post-zygotic isolation. Servedio and Noor include any detected increase in prezygotic isolation as reinforcement, as long as it is a response to selection against mating between two different species. Coyne and Orr contend that, "true reinforcement is restricted to cases in which isolation is enhanced between taxa that can still exchange genes".