From Local Adaptation to Speciation: Specialization and Reinforcement

Table 1

Classification of reinforcement mechanisms based on the life stage modified and their consequences on genetic associations involved in genetic clustering. This classification is orthogonal to the one- versus two-allele classification.

Life stage modified	Dispersal	Syngamy	Meiosis
Prominent biological example	Habitat choice	Mate choice	Sex/asex
Genetic clustering at local adaptation loci through^1	Increased frequency differences between habitats	Increased homozygosity	Increased linkage disequilibrium
Usual population genetic parameter measuring clustering	𝐹st (differentiation)	𝐹is(departure from Hardy-Weinberg)	D (linkage disequilibrium)
Primary effect of modifier on local adaptation loci	Change in frequency	Change in within-locus associations^2	Change in between-loci associations
Primary modifier association^3	𝐶ma,∅	𝐶ma,a	𝐶mab,∅
Increased differentiation	Directly	Indirectly^4	Indirectly^4
Notable complication preventing clustering^5	Kin selection	Recessivity^6	Negative epistasis
“One-allele” examples	An allele reducing dispersal or causing preference to natal habitat (Figure 2)	An allele causes assortment based on self-similarity (Figure 1)	An allele causes a reduction in recombination (Figure 4)
“Two-allele” examples	Allele 1 causes preference to habitat 1 and allele 2 to habitat 2	Allele 1 cause preference to phenotype 1 and allele 2 to phenotype  2^7	Allele 1 (inversion) causes linkage in group of genes 1 and allele 2 (noninversion) in group of genes 2

¹This would also apply to loci involved in genetic incompatibilities in a secondary contact.
²Unless mating is selective and causes a direct advantage to locally adapted alleles (i.e., it changes frequency at the local adaptation loci), as found in model involving sexual selection [8, 103].
³Notation as in [104, 105], where m is the modifier locus and a, b the local adaptation loci. ‘‘Primary’’ association refers to the fact that the phenotypic effect of the modifier causes first a direct change on the genetic composition of the population (on frequency, within or between loci associations), which may then change the efficacy of selection. Eventually, a modifier promoting clustering will end up associated to the beneficial allele locally (𝐶_ma,∅>0). See Figures 1, 2 and 4 for examples.
⁴Indirectly by increasing the variance in fitness and the efficacy of selection.
⁵Besides possible direct costs relative to the strategy used (e.g., cost of finding a mate or the right habitat). Different traits are exposed to a variety of other selective effects (see text).
⁶Which generates inbreeding depression.
⁷Phenotype 1 and 2 may result from alleles at the adaptation locus or to another unrelated marker trait. Similarly in a ‘‘one-allele’’ model, self-similarity may be evaluated in reference to a marker trait at another locus than the modifier or the local adaptation locus. In both cases, the marker trait has to diverge in the two incipient species, which is essentially a two-allele mechanism. Thus, with three locus like this, the one- versus two-allele distinction is made more complicated by the fact that the marker trait must diverge (two-allele), but the modifier of the strength of assortment need not (it can be one- or two-allele) [52]. Another complication of the one- and two-allele classification arises when the locus exposed to postzygotic selection also causes premating isolation (as seen in so-called “magic trait” models). This can be thought as the limit where the loci causing prezygotic isolation and postzygotic selection become confounded.