On Evolution

1. Genetic Differentiation during Speciation

Ever since Darwin, a central issue in evolutionary biology has been whether closely related species differ substantially or only trivially in their genetic features. In the s, molecular genetic techniques (notably protein electrophoresis) were introduced to population biology , and these procedures gave new opportunities to examine the topic of speciation empirically. This paper, written while Avise was a graduate student in Francisco Ayala’s laboratory at the University of California at Davis, addresses two allied but subtly distinct evolutionary questions that were important in the s and remain so today: What molecular genetic changes accompany the formation of new species, and what genetic changes are actually responsible for the origins of reproductive isolation? Readers wishing a superb update on speciation topics discussed in this early review should consult J. A. Coyne and H. A. Orr’s Speciation (). Biological evolution consists of two processes: anagenesis (or phyletic evolution) and cladogenesis (i.e., splitting). Anagenetic change is gradual and usually results from increasing adaptation to the environment . A favorable mutation or other genetic change arising in a single individual may spread to all descendants by natural selection. Cladogenesis results in the formation of independent evolutionary lineages. Favorable genetic changes arising in one lineage cannot spread to members of other lineages. Cladogenesis is responsible for the great diversity of the biological world, allowing adaptation to the variety of ways of life. The most decisive cladogenetic process is speciation. Among sexually reproducing organisms, species are groups of interbreeding natural populations that are reproductively isolated from other such groups. Gene exchange can occur among Mendelian popuGenetic Differentiation during Speciation 1 lations of the same species. The speciation process requires the development of reproductive isolation between populations, resulting in independent gene pools. Two related questions concerning speciation interest evolutionists: What ecological and evolutionary conditions promote speciation, and what changes in the genetic composition of populations result in reproductive isolation? For sexually reproducing organisms, isolation by geographic barriers and the concomitant severe restriction of gene exchange is the usual prerequisite to genetic divergence and speciation. Geographically isolated populations accumulate genetic differences as they adapt to their different environments (or sometimes as they merely drift apart in genetic composition). In the short run, they may become recognizable as races. However, not all races will become species because the process of geographic differentiation is reversible. If the races have not sufficiently diverged while separated (allopatric), they may later converge or fuse through hybridization. On the other hand, allopatric populations may sometimes become sufficiently different genetically, so that if the opportunity for gene exchange ensues again, hybrids will have low fitness. Natural selection would, then, favor the completion of reproductive isolation. Geographic Speciation Two stages may be recognized in the process of geographic speciation. During the first stage, populations become isolated by geographic barriers and accumulate genetic differences. Much of this divergence is the result of adaptation to different environments, but other factors such as genetic drift and founding events may play a role. Partial or even complete reproductive isolation between populations may develop as a by-product of this genetic divergence. During the second stage of speciation, natural selection may hasten the direct development of reproductive isolation in the form of prezygotic isolating barriers. This stage begins when genetically differentiated populations regain geographic contact. If reproductive isolation is not yet complete and if the gene pools have sufficiently diverged, matings be-  On Evolution tween individuals of different populations may produce progenies of reduced quality (thus, lower fitness). Natural selection would then favor genetic variants that promote matings between members of the same population. Reproductive isolation would thereby be enhanced. Two survey strategies have been employed in attempts to determine the degree of genetic differentiation during speciation. A direct strategy involves assaying populations that appear to be in various stages of the speciation process. Such studies permit assessment of the amount of genetic differentiation during the first stage of speciation when allopatric populations develop incipient reproductive isolation , and during the second stage of speciation when reproductive isolation is being completed by natural selection between populations that have reconnected (regained sympatry). A second survey strategy involves assaying populations belonging to different species. Species’ differences represent the sum of genetic differences accumulated subsequent to speciation as well as during the speciation process itself. Hence, interest has centered on species that by other...