GENETIC ARCHITECTURE OF DIVERGENCE: THE SELFING SYNDROME INIPOMOEA LACUNOSA

Abstract

Premise of the studyHighly selfing plant species frequently display a distinctive suite of traits termed the “selfing syndrome.” This study tests the hypothesis that these traits are grouped into correlated evolutionary modules and determines the degree of independence between such modules.MethodsWe evaluated phenotypic correlations and QTL overlaps in F2 offspring of a cross between the morning glories Ipomoea lacunosa and I. cordatotriloba and investigated how traits clustered into modules at both the phenotypic and genetic level. We then compared our findings to other QTL studies of the selfing syndrome.Key resultsIn the I. lacunosa selfing syndrome, traits group into modules that display correlated evolution within but not between modules. QTL overlap predicts phenotypic correlations, and QTLs affecting the same trait module are significantly physically clustered in the genome. The genetic architecture of the selfing syndrome varies across systems, but the pattern of stronger within-than between-module correlation is widespread.ConclusionsThe genetic architecture we observe in the selfing syndrome is consistent with a growing understanding of floral morphological integration achieved via pleiotropy in clustered traits. This view of floral evolution is consistent with resource limitation or predation driving the evolution of the selfing syndrome, but invites further research into both the selective causes of the selfing syndrome and how genetic architecture itself evolves in response to changes in mating system.

Modularity and selection of nectar traits in the evolution of the selfing syndrome in Ipomoea lacunosa (Convolvulaceae)

“…Two previous QstFst studies determined that natural selection contributed to the divergence of five floral size and two nectar traits between Ipomoea lacunosa and I. cordatotriloba (Duncan & Rausher, 2013b;Rifkin et al, 2019bRifkin et al, , 2021. However, neither study was able to distinguish between selection acting directly on these characters and indirect selection due to correlations with selected characters.…”

“…The flowers of Ipomoea lacunosa and I. cordatotriloba consist of at least two distinct evolutionary modules: floral size traits and nectar traits. A previous study of these species only examined one nectar trait (nectar volume), which clustered with floral size traits (Rifkin et al, 2021). By including additional nectar traits, we could distinguish these modules by the moderately high within-module genetic correlations, but low betweenmodule correlations (Table 2a).…”

“…Markers determined from ddRAD sequencing reads were aligned to the draft I. lacunosa genome using NextGenMap (Sedlazeck et al, 2013), and a linkage map for F5 individuals was constructed concurrently with F2 individuals (Rifkin et al, 2021) using Lep-Map3 (Rastas, 2017;Methods S3). This process resulted in a total of 6056 markers with 174-625 markers per linkage group (Supporting Information Fig.…”

“…Although several studies have identified quantitative trait loci (QTLs) to assess the degree to which the evolution of different syndrome traits have evolved in a correlated fashion, most have focused on herkogamy, floral size, time to flowering, and pollen size and number (Rifkin et al, 2021). Because only one examined nectar production (nectar volume; Rifkin et al, 2021), the extent to which nectar traits constitute a distinct evolutionary module remains to be examined. In this study, we address this issue for a pair of morning glory species, Ipomoea cordatotriloba and its highly selfing sister species I. lacunosa, which exhibits the selfing syndrome.…”

“…The repeated evolution of the selfing syndrome (Barrett, 2002;Arunkumar et al, 2015) has fostered studies of its evolution in a wide range of flowering species, including Capsella (Slotte et al, 2012;Sas et al, 2016;Fujikura et al, 2017;Wozniak et al, 2020), Collinsia (Baldwin et al, 2011;Strandh et al, 2017;Frazee et al, 2021), Mimulus (Fenster & Ritland, 1994;Fishman et al, 2002Fishman et al, , 2015, and Ipomoea (Duncan & Rausher, 2013b;Rifkin et al, 2019bRifkin et al, , 2021. Although several studies have identified quantitative trait loci (QTLs) to assess the degree to which the evolution of different syndrome traits have evolved in a correlated fashion, most have focused on herkogamy, floral size, time to flowering, and pollen size and number (Rifkin et al, 2021). Because only one examined nectar production (nectar volume; Rifkin et al, 2021), the extent to which nectar traits constitute a distinct evolutionary module remains to be examined.…”