Evolution of Autonomous Selfing in Marginal Habitats: Spatiotemporal Variation in the Floral Traits of the Distylous Primula wannanensis

Abstract

Outcrossing plant species are more likely to exhibit autonomous selfing in marginal habitats to ensure reproduction under conditions of limited pollinator and/or mate availability. Distyly is a classical paradigm that promotes outcrossing; however, little is known about the variation in floral traits associated with distylous syndrome in marginal populations. In this study, we compared the variation in floral traits including stigma and anther height, corolla tube length, herkogamy, and corolla diameter between the central and peripheral populations of the distylous Primula wannanensis, and assessed the variation of floral traits at early and late florescence stages for each population. To evaluate the potential consequences of the variation in floral traits on the mating system, we investigated seed set in each population under both open-pollinated and pollinator-excluded conditions. The flower size of both short- and long-styled morphs was significantly reduced in late-opening flowers compared with early opening flowers in both central and peripheral populations. Sex-organ reciprocity was perfect in early opening flowers; however, it was largely weakened in the late-opening flowers of peripheral populations compared with central populations. Of these flowers, disproportionate change in stigma height (elongated in S-morph and shortened in L-morph) was the main cause of reduced herkogamy, and seed set was fairly high under pollinator-excluded condition. Our results provide empirical support for the hypothesis on the evolution of delayed autonomous selfing in marginal populations of distylous species. Unsatisfactory pollinator service is likely to have promoted reproductive assurance of distylous plants with largely reduced herkogamy mimicking “homostyles.”

The rapid appearance of homostyly in a cultivated distylous population of Primula forbesii

“…Through this approach, long homostyly might arise directly from the variations of the stamen of L‐morph or pistil of S‐morph, and it possesses pollen size, stigma papillae, and self‐incompatibility similar to L‐ or S‐morphs (Brys & Jacquemyn, 2015 ; Ganders, 1979 ; Mather & de Winton, 1941 ). Additionally, the long homostyly caused by polygenic modifiers would present strong variations of sexual organ height (Zhang et al, 2021 ).…”

“…In numerous families, the shift of mating system will affect the biodiversity, the response to selection, the evolution of floral signals and rewards, and the population structure (Charlesworth & Charlesworth, 1979 ; de Vos et al, 2014 ; Sicard & Lenhard, 2011 ; Yuan et al, 2017 ; Zeng et al, 2022 ). This transition has a profound ecological, evolutionary, and genetic influence on plant populations because it leads to reproductive isolation and subsequent speciation (Wright et al, 2013 ), which are interesting to biologists since Darwin's seminal research (Darwin, 1877 ; Yuan et al, 2019 ; Zhang et al, 2021 ; Zhou et al, 2017 ). Of special value for investigations of mating system changes are lineages that include outcrossing and self‐pollination, which provide a valuable opportunity to determine the selection forces and evolutionary consequences of selfing transitions.…”

“…The hypothesis of reproductive assurance explains the occurrence of homostyly in heterostylous populations (Darwin, 1876), in which due to the unreliable service of pollinators and the limited number of pollen donors in extreme environments or colonizing episodes, the transition to self‐pollination is conducive (Brys & Jacquemyn, 2015; Busch & Delph, 2012; Moeller, 2006; Shao et al, 2019; Yuan et al, 2017; Zhang et al, 2021). Homostyly formation may also follow long‐distance dispersal and establishment of polyploid (Barrett et al, 2009; Barrett & Shore, 1987; Naiki, 2012).…”

Habitat fragmentation affects climate adaptation in a forest herb

“…climate adaptation, climate change, common garden, drought stress, habitat fragmentation, local adaptation, mating systems, phenotypic plasticity, plant conservation, plant traits evolutionary breakdown of herkogamy can lead to feedback loops, as reduced herkogamy can drive increasing levels of autonomous selfing (Herlihy & Eckert, 2007;Zhang et al, 2021). This may be beneficial when pollination is limited, but it can also increase inbreeding and reduce genetic diversity (Jacquemyn et al, 2012;Porcher & Lande, 2005).…”

 Primula xinningensis (Primulaceae), a new species from karst caves in Hunan, China

“…This section now includes P. ranunculoides F.H.Chen, P. cicutariifolia Pax, P. jiugongshanensis J.W.Shao, P. hubeiensis X.W.Li and P. merrilliana complex ( Shao et al 2012 ; He et al 2017 ; Li et al 2018 ; He et al 2021 ). They are all endemic to central or eastern China and often grow at the waterside or the edge of broadleaf deciduous forests between 50 and 1600 m ( Shao et al 2012 ; He et al 2017 ; Zhang et al 2021 ).…”