Directional selection is the primary cause of phenotypic diversification

Abstract

Selection is widely accepted as the principal force shaping phenotypic variation within populations. Its importance in speciation and macroevolution has been questioned, however, because phenotypic differences between species or higher taxa sometimes appear to be nonadaptive. Here, we use the quantitative trait locus (QTL) sign test to evaluate the importance of directional selection in phenotypic divergence. If a trait has a history of directional selection, QTL effects should be mostly in the same direction; otherwise QTLs with antagonistic effects should be common. Analysis of QTL effects for 572 traits from 86 studies revealed significantly fewer antagonistic QTLs than expected under neutrality, a result that validates Darwin's claim that phenotypic diversification is caused mainly by selection. Moreover, interspecific trait differences were more strongly or consistently selected than intraspecific differences, strengthening a growing consensus among students of speciation that directional selection is the primary cause of speciation. Contrary to studies of selection in contemporary populations, life history traits appear to be selected more strongly than morphological traits, but traits related to the timing of development are weakly selected relative to most other traits. It is often lamented that studies of present-day populations provide only the briefest snapshot of evolution and tell us little about the evolutionary forces that have shaped a particular trait or organism in the past (1). Although ancestral phenotypes can be reconstructed with phylogenetic methods (2) or directly determined from fossils (3), neither approach reveals the evolutionary processes that created these phenotypes. Even if these historical data could help, there is considerable uncertainty associated with the reconstruction of ancestral character states (4), and a fossil record is missing for most taxa and incomplete for others. As a result, a direct link between the action of microevolutionary forces detected in studies of contemporary populations and patterns of speciation and macroevolution has been difficult to make (1), yet this is a central problem in evolutionary biology.A possible method for reconstructing the selective history of complex traits has, however, recently been proposed (5). The method is based on the direction of effects of quantitative trait loci (QTLs) that contribute to phenotypic differences. If a trait has had a continuous history of directional selection, then QTL effects should be in the same direction within a line. In contrast, if a trait has diverged under neutrality, QTLs with opposing or antagonistic effects should be common. This approach has been formalized as the QTL sign test (5), which compares the proportion of antagonistic QTLs in a given line with those predicted under neutral conditions.In this article, we review the QTL literature to estimate the distribution of plus and minus QTL alleles for different kinds of organisms and for different kinds of traits. Three comparisons were of partic...

The genetic architecture necessary for transgressive segregation is common in both natural and domesticated populations

“…(a) Representation of organisms and traits Out of the 96 studies included in this review, 27 (28%) concerned animals and 69 (72%) concerned plants (electronic Appendix A; Rieseberg et al 2002). Likewise, only 96 out of 749 traits scored (13%) were from animal studies compared with 653 traits (87%) from plants (table 2).…”

Quantitative Trait Locus Analysis of the Early Domestication of Sunflower

“…While data on QTL directionality can be used to statistically test for past directional selection (Orr 1998), the power of this approach is limited by QTL numbers. Thus, following the methods of Rieseberg et al (2002), we pooled our data across traits and tested for selection on the domestication syndrome as a whole. In this case, the results were highly significant (P , 0.001), providing clear evidence that sunflower domestication was driven by consistent directional selection on a wide variety of traits.…”

The genetic basis of speciation in the Giliopsis lineage of Ipomopsis (Polemoniaceae)

“…Although random genetic drift has long been proposed as a key mechanism in shaping the phenotypic differences that evolve during speciation (Wallace, 1889), a growing body of direct empirical evidence suggests that natural selection is the primary cause of the phenotypic differences between species (Rieseberg et al, 2002;Louthan and Kay, 2011). Such selection can be caused by various biotic and abiotic factors (Rieseberg and Willis, 2007).…”