Cytoplasmic male sterility in Mimulus hybrids has pleiotropic effects on corolla and pistil traits

Abstract

The mechanisms underlying genetic associations have important consequences for evolutionary outcomes, but distinguishing linkage from pleiotropy is often difficult. Here, we use a fine mapping approach to determine the genetic basis of association between cytonuclear male sterility and other floral traits in Mimulus hybrids. Previous work has shown that male sterility in hybrids between Mimulus guttatus and Mimulus nasutus is due to interactions between a mitochondrial gene from M. guttatus and two tightly linked nuclear restorer alleles on Linkage Group 7, and that male sterility is associated with reduced corolla size. In the present study, we generated a set of nearly isogenic lines segregating for the restorer region and male sterility, but with unique flanking introgressions. Male-sterile flowers had significantly smaller corollas, longer styles and greater stigmatic exsertion than fertile flowers. Because these effects were significant regardless of the genotypic composition of introgressions flanking the restorer region, they suggest that these floral differences are a direct byproduct of the genetic incompatibility causing anther abortion. In addition, we found a non-significant but intriguing trend for male-sterile plants to produce more seeds per flower than fertile siblings after supplemental pollination. Such pleiotropic effects may underlie the corolla dimorphism frequently observed in gynodioecious taxa and may affect selection on cytoplasmic male sterility genes when they initially arise.

Prolonged stigma and flower lifespan in females of the gynodioecious plant Geranium sylvaticum

“…Flower size on the other hand seems to be determined more by the level of male functionality, possibly due to a strong developmental correlation between the stamens and petals, because of a genetic linkage or pleiotropic effects (Raab and Koning, 1988;Schultz, 2003;Barr and Fishman, 2011), even though we did not find a correlation between the number of functional anthers and flower size within the intermediates.…”

“…In fact, female flowers are almost always smaller than hermaphrodite flowers (reviewed in Delph, 1996 andShykoff et al, 2003;e.g. Bai et al, 2011;Barr and Fishman, 2011;Cuevas and López, 2011;Griffin and Byers, 2012;Blank et al, 2014;Cuevas et al, 2014) and/or they produce less nectar and pollen, leading to lower pollinator visitation rates (Delph, 1996;Ashman, 2000;Bai et al, 2011). On the other hand, the smaller size and number of flowers of female plants may also render them less attractive to enemies like florivores or seed herbivores, leading to a relatively higher seed output in females than hermaphrodites (Marshall and Ganders, 2001;Ashman, 2002;Asikainen and Mutikainen, 2005a;Collin and Shykoff, 2009;Clarke and Brody, 2015).…”

The genetic architecture of traits associated with the evolution of self‐pollination in Mimulus

“…Consistent with this possibility, c. 40% of Capsella F 2 flowers exhibited homeotic abnormalities (often seen in hybrid CMS), and the largest QTL for floral aberration (table 2 in Slotte et al, 2012) overlapped with the leading QTLs for both male and female reproductive traits. Our results in Mimulus (Barr & Fishman, 2011; this study) suggest that sterility commonly affects floral traits in hybrids, and argue for the explicit consideration of the pleiotropic effects of hybrid sterility in future investigations of the genetic basis of floral trait divergence.…”

“…In measuring floral traits, we also discovered that a fraction of M. parishii 9 M. lewisii F 2 hybrids were completely male sterile, making deformed anthers with little or no pollen. Male sterility, and especially hybrid anther sterility (Barr & Fishman, 2011), often has pleiotropic effects on floral morphology (reviewed in Chase, 2007), so we then asked whether anther sterility QTLs were coincident with (and probably causal of) floral QTLs. If so, this could be a general confounding factor in estimating the genetic architecture of floral traits.…”

Mitochondrial Genome Evolution and Gynodioecy

“…Remember that to spread, females must benefit from the loss of pollen production by producing more or better seeds. Barr and Fishman (2011) showed that male sterility had negative pleiotropic effects on corolla size, male-sterile plants had smaller flowers, but also positive effects on female traits such as the style length and thus better exposure of style and stigma, and a marginal increase in seed production. The question remains how restorer alleles succeeded in spreading to the whole species until their complete fixation in the species, since only interspecies crosses revealed male sterility.…”