Genetic architecture of divergence: the selfing syndrome in Ipomoea lacunosa

Abstract

Highly selfing plant species frequently display a distinctive suite of traits termed the selfing syndrome. Here we tested the hypothesis that these traits are grouped into correlated evolutionary modules and determined the degree of independence between such modules. Methods: We 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. Results: In the I. lacunosa selfing syndrome, traits grouped into modules that displayed correlated evolution within but not between modules. QTL overlap predicted phenotypic correlations, and QTLs affecting the same trait module were significantly physically clustered in the genome. The genetic architecture of the selfing syndrome varied across systems, but the pattern of stronger within-than between-module correlation was widespread. Conclusions: The 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.

How broad is the selfing syndrome? Insights from convergent evolution of gene expression across species and tissues in the Capsella genus

“…As pointed out by Cutter (2019), deciphering the relative contribution of adaptive changes vs relaxed selection for any trait individually remains challenging and few studies have attempted it. In morning glory (Ipomoea lacunosa), Rifkin et al (2021) used Q ST -F ST comparisons to identify selection associated to the divergence between selfers and outcrossers on traits ranging from corolla size to early growth. Divergence between selfers and outcrossers was found to be under selection for corolla size and nectar traits, but not for early growth or pollen traits.…”

“…This pattern is not explained by some ubiquitous genes given the small overlap that we found between the three tissues. One central question is whether selfing syndrome trait evolution arises from relaxed selection (random genetic drift), from adaptive re-allocation of resources or from a mixture of both (Cutter, 2019;Rifkin et al, 2021;Tsuchimatsu & Fujii, 2022). As pointed out by Cutter (2019), deciphering the relative contribution of adaptive changes vs relaxed selection for any trait individually remains challenging and few studies have attempted it.…”

“…In particular, self‐fertilizing plant species no longer need to attract pollinators and are characterized by reduced flowers, and a low production of pollen, nectar and scent compared to their outcrossing relatives (Carr & Eubanks, 2002 ; Koslow & DeAngelis, 2006 ). Altogether, the most conspicuous changes associated with the transition from outcrossing to selfing have been called the selfing syndrome (Sicard & Lenhard, 2011 ; Rifkin et al ., 2019 , 2021 ; Tsuchimatsu & Fujii, 2022 ), and there is evidence of convergent evolution across species, at least for floral traits (Woźniak et al ., 2020 ). Given the major impact of the shift from outcrossing to selfing on genetic diversity, population ecology and dynamics, one would expect the shift in mating system to also alter basic genomic processes such as gene expression (Thomas et al ., 2012 ; Cutter, 2019 ), and therefore to affect phenotypic traits beyond those directly related to reproduction.…”

“…Generally, one would expect traits specifically related to reproduction to be more strongly affected by mating system shift than less related traits. Traits associated with the shift in mating system can evolve as a direct or indirect – in the case of correlated response – adaptation to the new conditions associated with self‐fertilization, that can be viewed as a new phenotypic optimum, and/or because the selection pressure associated with outcrossing is relaxed (Cutter, 2019 ; Rifkin et al ., 2021 ; Tsuchimatsu & Fujii, 2022 ). Relaxed selection can take many forms (Lahti et al ., 2009 ).…”

Modular regulation of floral traits by aPRE1homolog inMimulus verbenaceus: implications for the role of pleiotropy in floral integration

“…Pleiotropy and modularity may have played a critical role in the evolutionary diversification of organismal forms in general [ 21 , 22 , 24 ] and flower form and function in particular [ 9 , 44 ], because selection on one trait will result in correlated changes in functionally related traits. Indeed, floral traits associated with pollinator shifts have been subjected to quantitative trait locus (QTL) analysis in a wide range of sympetalous taxa, including Mimulus [ 11 , 46 ], Leptosiphon [ 47 ] , Ipomopsis [ 48 ], Penstemon [ 18 ], Petunia [ 49 ], and Ipomoea [ 50 ]. These studies showed that corolla tube, stamen, and style lengths are not only genetically correlated but also frequently co-localized to the same QTL, consistent with a role of pleiotropic QTLs underlying intra-floral integration and in facilitating rapid floral form diversification.…”