Speciation

From NECSIWiki

A major issue in speciation theory is defining a species. The classic definition that serves as the standard against which all other definitions are compared is Ernst Mayr’s Biological species concept. Mayr defines a species to be a group of actually or potentially interbreeding organisms that is reproductively isolated from other such groups (Mayr 1963). Under this view, a species is a set of organisms that shares a common gene pool. From a practical perspective it is fraught with problems. These include defining what is meant by “potentially interbreeding”, how to deal with asexual organisms, and the fact that “interbreeding” is normally difficult or impossible to test, especially in preserved museum specimens. Other species definitions generally fall into the classes of being “recognition” species definitions – two organisms are the same species if they recognize each other as being the same species (the biological species concept is a recognition definition), “morphological” species definitions – two organisms are the same species if they look similar, “evolutionary” and “ecological” species definitions – two organisms are the same species if they share the same evolutionary or ecological history, and “phylogenetic” species definitions – two organisms are the same species if they are related through descent (e.g., Templeton 1989).

Models of speciation can be divided into two classes. The more familiar are what might be called “ecological” models. Perhaps less familiar are the “genetic” models. Discussions of models of speciation frequently address these two types models as if they are directly comparable, resulting in far more confusion than is necessary. For the current discussion I will use Ernst Mayr’s Biological Species concept.

Ecological Models of Speciation: In ecological models of speciation it is generally assumed that speciation will occur when (1) two populations become reproductively isolated for ecological reasons, and (2) a sufficiently long period of time has passed. In general, no specific mechanism leading to speciation is explicitly postulated. Coyne and Orr (2004) provide a good review of this class of models. In most cases there is an implicit assumption that selective pressures in the two populations, or that some form of genetic incompatibility will arise by mutation once the populations are isolated (see the Bateson-Dobzhansky-Muller model below). These models focus on the ecological processes that lead to reproductive isolation. The classic example of this class of models is Mayr’s allopatric model of speciation (Mayr 1963). In this model a single population becomes divided into two geographically isolated populations when an ecological barrier is imposed. Such a barrier might be a river or mountain range forming. The resulting populations are reproductively isolated because of this barrier, and as a result over time evolve to become separate species. Variants on the allopatric model of speciation are parapatric models in which there is a zone of contact between the two populations, and peripatric in which one of the populations is a peripheral isolate of the other. These models tend not to be controversial, as it is generally accepted that if two populations remain separated for a sufficiently long period of time they will become different species. More controversial is sympatric speciation in which a single population divides into two populations in the same geographic region. Typical of these models are the proposed method of speciation for Rhagoletis pomonella sibling species complex, although some have argued that this system is an example of micro-allopatric speciation. Some members of this species complex oviposit on hawthorn, whereas other members of the complex oviposit on apple. This difference in oviposition preference is based on genetically based responses to scent cues for the different fruits. In this genus mating takes place on the host fruit shortly after emergence of the female. Thus, even though apples and hawthorns occupy the same habitat the two sibling species are reproductively isolated because of differences in where mating takes place (e.g., Bush and Smith 1998). Many question whether realistic sympatric models of speciation can have sufficient reproductive isolation for speciation to occur, however, the basic tenet of reproductive isolation and time remain the underlying elements for these models.

Genetic Models of Speciation: In contrast to the ecological models of speciation, the genetic models generally assume that ecological reproductive isolation exists, and then examine the genetic mechanism leading to genetic incompatibility. These models also fall into two categories, those models that postulate new genetic mutations that occur after the separation of the two populations, and those that postulate that speciation occurs as a result of genetic variation that was present prior to the division of the ancestral population.

Models that assume that speciation occurs as a result of new mutations can generally be considered to be a variant of the Bateson-Dobzhansky-Muller model (Orr 1995, Johnson 2002). In this model a minimum of two mutations occur in one population, or one in each of the two isolated populations. If both mutations occur in a single population then the first is neutral or beneficial in either population, however the second, while compatible with the first mutation, is incompatible with the ancestral genetic system (represented in the other population) lacking the first mutation. If the mutations occur in separate populations then they are both compatible with the ancestral genetic system, but mutually incompatible. The important points about these models is that it takes a minimum of two mutations for the genetic incompatibility to arise, and that some form of genetic interaction (epistasis) is required. This does not preclude the possibility that it may take more than two mutations. Indeed, Orr has shown that the probability of speciation (defined as genetic incompatibility) increases with time because as mutations accumulate there will be an increased probability that an incompatibility will arise.

Models that allow for speciation due to genetic variance in the ancestral population have, until recently, been far more speculative. These models postulate that there is some change that occurs in the genetic or physical environment in one population that causes it to rapidly evolve to a new genetic system. A classic example of this is the founder-flush speciation model put forth by Carson (Carson and Templeton 1984). In this model a small number of individuals, perhaps a single gravid female, founds a new population, potentially in a new environment. The very small population size causes a random change in gene frequency. The founding population goes through a “flush” phase in which the population is released from competition and predation because of its new environment and initially small population size. During this phase novel genotypes can survive since selection is relaxed. Finally, the population adapts to the new genetic and physical environment, in the process becoming a new species. This radical genetic transition has been termed a “genetic revolution” (Mayr 1963) or a “genetic transilience” (Carson and Templeton 1984). These models have been very controversial, in no small part because classic population genetic theory contains nothing that would support a model of genetic revolutions (Barton and Charlesworth 1984). More recent models of epistasis in structured populations (Wade and Goodnight 1998) lend more credence to these models of speciation, however, much work remains before we have a firm understanding of how standing variation within a population can lead to speciation following population subdivision.

Other models of speciation: The models discussed above are the major classes of speciation models that are generally considered. There are numerous other models that defy such easy classification. These include models of the role of hybridization in speciation, speciation models related to chromosomal changes (White 1978, Rieseberg, L. 2001), and models involving selective divergence (see Coyne and Orr 2004). Finally, the models described fall within classic population genetics traditions. None of the models, with the possible exception of those based on standing genetic variation rely on modern complexity theory. Recent unpublished work suggests that new models of speciation may arise when spatial structure and limited gene flow are coupled with gene interaction.

G. L. Bush and J. Smith. 1998. The genetics and ecology of sympatric speciation: a case study. Researches on Population Ecology, 40: 175-187.

Mayr, E. 1963. Animal species and evolution. Belknap Press of Harvard University Press, Cambridge, Massachusetts.

Orr, H. A., 1995 The population genetics of speciation: the evolution of hybrid incompatibilities. Genetics 139:1805-1813 http://www.genetics.org/cgi/content/abstract/139/4/1805?ijkey=e7cbe11030f9087dd84cc15c937b1c5b4e3e83a9