A polygenic architecture with conditionally neutral effects underlies ecological differentiation in Silene

Abstract

Ecological differentiation can drive speciation but it is unclear how the genetic architecture of habitat-dependent fitness contributes to lineage divergence. We investigated the genetic architecture of cumulative flowering, a fitness component, in second-generation hybrids between Silene dioica and S. latifolia transplanted into the natural habitat of each species. We used reduced-representation sequencing and Bayesian Sparse Linear Mixed Models (BSLMMs) to analyze the genetic control of cumulative flowering in each habitat. Our results point to a polygenic architecture of cumulative flowering. Allelic effects were mostly beneficial or deleterious in one habitat and neutral in the other. The direction of allelic effects was associated with allele frequency differences between the species: positive-effect alleles were often derived from the native species, whereas negative-effect alleles, at other loci, tended to originate from the non-native species. We conclude that ecological differentiation is governed and maintained by many loci with small, conditionally neutral effects. Conditional neutrality may result from differences in selection targets in the two habitats and provides hidden variation upon which selection can act. Polygenic architectures of adaptive differentiation are expected to be transient during lineage divergence and may therefore be unrelated to high genetic differentiation at the underlying loci.

Polygenic routes lead to parallel altitudinal adaptation in Heliosperma pusillum (Caryophyllaceae)

“…Consistently, a polygenic architecture of adaptive differentiation was uncovered also in Silene (Gramlich et al, 2021), a close relative of Heliosperma.…”

“…In line with other studies on diverse organisms including whitefish (Rougeux et al, 2019 ), hummingbirds (Lim et al, 2019 ), snails (Ravinet et al, 2016 ) and frogs (Sun et al, 2018 ), our results suggest that convergent phenotypes can be achieved via changes in different genes affecting the same molecular pathway and, ultimately, adaptive traits, and that this polygenic basis might facilitate repeated adaptation to different elevations via alternative routes. Consistently, a polygenic architecture of adaptive differentiation was uncovered also in Silene (Gramlich et al, 2021 ), a close relative of Heliosperma .…”

Using singleton densities to detect recent selection inBos taurus

“…The release of these data spurred a series of studies and new methods designed specifically to detect polygenic selection. These methods usually involve determining which SNPs affecting a phenotype show correlated changes in frequency (Berg & Coop, 2014 ; Racimo et al., 2018 ; Sanjak et al., 2018 ; Josephs et al., 2019 ; Berg et al., 2019a , 2019b ; Uricchio et al., 2019 ; Edge & Coop, 2019 ; Kreiner et al., 2020 ; Wieters et al., 2021 ; Gramlich et al., 2021 ); which sets of alleles are associated with certain environmental or climatic variations (Coop et al., 2010 ; Turchin et al., 2012 ; Robinson et al., 2015 ; Yeaman et al., 2016 ; Exposito‐Alonso et al., 2018 ; Zan & Carlborg, 2018 ; Exposito‐Alonso et al., 2019 ; MacLachlan et al., 2021 ; Ehrlich et al., 2021 ; Fuhrmann et al., 2021 ; Rowan et al., 2021 ); or determining which SNPs or genetic regions explain a large fraction of phenotypic variance and trait heritability (Zhou et al., 2013 ; Yang et al., 2015 ; Gazal et al., 2017 ; Zeng et al., 2018 ; Schoech et al., 2019 ; Exposito‐Alonso et al., 2020 ; Duntsch et al., 2020 ; Zeng et al., 2021 ). Some of these approaches use overlapping methods.…”