The genic view of the process of speciation

Abstract

The unit of adaptation is usually thought to be a gene or set of interacting genes, rather than the whole genome, and this may be true of species differentiation. Defining species on the basis of reproductive isolation (RI), on the other hand, is a concept best applied to the entire genome. The biological species concept (BSC; Mayr, 1963) stresses the isolation aspect of speciation on the basis of two fundamental genetic assumptions – the number of loci underlying species differentiation is large and the whole genome behaves as a cohesive, or coadapted genetic unit. Under these tenets, the exchange of any part of the genomes between diverging groups is thought to destroy their integrity. Hence, the maintenance of each species’ genome cohesiveness by isolating mechanisms has become the central concept of species. In contrast, the Darwinian view of speciation is about differential adaptation to different natural or sexual environments. RI is viewed as an important by product of differential adaptation and complete RI across the whole genome need not be considered as the most central criterion of speciation. The emphasis on natural and sexual selection thus makes the Darwinian view compatible with the modern genic concept of evolution. Genetic and molecular analyses of speciation in the last decade have yielded surprisingly strong support for the neo‐Darwinian view of extensive genetic differentiation and epistasis during speciation. However, the extent falls short of what BSC requires in order to achieve whole‐genome ‘cohesiveness’. Empirical observations suggest that the gene is the unit of species differentiation. Significantly, the genetic architecture underlying RI, the patterns of species hybridization and the molecular signature of speciation genes all appear to support the view that RI is one of the manifestations of differential adaptation, as Darwin (1859, Chap. 8) suggested. The nature of this adaptation may be as much the result of sexual selection as natural selection. In the light of studies since its early days, BSC may now need a major revision by shifting the emphasis from isolation at the level of whole genome to differential adaptation at the genic level. With this revision, BSC would in fact be close to Darwin’s original concept of speciation.

To be or not to be a hamlet pair in sympatry

“…1). This fits well with the idea that genomes can be rather 'porous' with respect to gene flow in neutral markers (Wu 2001). Similarly, in the simulations by Gavrilets & Vose (2005), the different virtual species maintained their divergence in selected loci despite of substantial gene flow at neutral loci.…”

Patterns of genetic diversity and differentiation in resistance gene clusters of two hybridizing European Populus species

“…In plants, resistance genes have been put forward for their potential role in the origin and maintenance of reproductive barriers through hybrid necrosis (Bomblies and Weigel 2007;Bomblies 2009). The two European Populus species, Populus alba and Populus tremula, have been described as species with incomplete reproductive barriers that hybridize despite relatively high levels of genomic divergence Lindtke et al 2012;Stölting et al 2013), largely concordant with available models of Bporous genomes^and heterogenous genomic divergence (Wu 2001;Feder et al 2012). Postzygotic selection has recently been put forward as a mechanism potentially maintaining the species barrier, but the exact selective factors acting on hybrid seedlings are currently unknown (Lindtke et al 2014).…”

“…Studying the genomics of taxa with Bporous genomes^provides an opportunity to obtain insights into the genetics of adaptation, reproductive isolation, and speciation (Wu 2001;Lexer and Widmer 2008;Feder et al 2012). During the process of Bspeciation with gene flow,^reproductive isolation evolves gradually from specific isolated genome regions of different sizes (genomic islands or continents of speciation) to complete genomic isolation and post-speciation divergence (Feder et al 2012).…”

The genomic landscape of species divergence in Ficedula flycatchers

“…Divergence is likely to start from specific loci that may precede and cause the evolution of reproductive incompatibility. Hybridization between diverging lineages may therefore create a genomic mosaic of regions where interspecific gene flow occurs at different rates (the genic view of speciation 11 ), with introgression expected to be weak in genomic regions involved in speciation. Revealing the genomic regions with elevated levels of divergence will eventually deepen our knowledge of the speciation process.…”