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Ecological Correlates and Genetic Consequences of Evolutionary Transitions from Distyly to Homostyly

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Ecological Correlates and Genetic Consequences of Evolutionary Transitions from Distyly to Homostyly Annals of Botany 120: 775–789, 2017 doi:10.1093/aob/mcx098, available online at https://academic.oup.com/aob PART OF A SPECIAL ISSUE ON MORPHOLOGY AND ADAPTATION Ecological correlates and genetic consequences of evolutionary transitions from distyly to homostyly Shuai Yuan1,2, Spencer C. H. Barrett3, Tingting Duan1,4, Xin Qian1,2, Miaomiao Shi1,* and Dianxiang Zhang1,* 1Key Laboratory of Plant Resources Conservation and Sustainable Utilization, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, China, 2University of Chinese Academy of Sciences, Beijing 10049, China, 3Department of Ecology and Evolutionary Biology, University of Toronto, 25 Willcocks St., Toronto, Ontario, Canada, M5S 3B2 and 4Guangdong Ocean University, Zhanjiang 524088, China *For correspondence: [email protected] or [email protected] Received: 8 April 2017 Returned for revision: 29 July 2017 Editorial decision: 6 July 2017 Accepted: 29 July 2017 Published electronically: 15 September 2017 • Background and Aims The outbreeding floral polymorphism heterostyly frequently breaks down, resulting in the evolution of self-fertilization as a result of homostyle formation. Here, the loss of floral polymorphism in distylous Primula oreodoxa, a sub-alpine species restricted to western Sichuan, China, was examined by investigating the ecological correlates and genetic consequences of mating system transitions. Several key questions were addressed. (1) What are the frequencies, geographical distribution and reproductive characteristics of floral morphs in distylous and homostylous populations? (2) Does increased elevation influence pollinator service and the likelihood of inbreeding in populations? (3) How often has homostyly originated and what are the consequences of the breakdown of distyly for the amounts and distribution of genetic diversity in populations? • Methods Fourteen populations throughout the range of P. oreodoxa were sampled, and morph frequencies and floral characteristics were recorded. Polymorphism at microsatellite loci and chloroplast DNA (cpDNA) variation were used to quantify population genetic structure and genetic relationships among populations. Controlled pollinations and studies of pollen tube growth and fertility were conducted to determine the compatibility status of populations and their facility for autonomous self-pollination. Finally, visitation rates of long- and short- tongued pollinators to distylous and homostylous populations at different elevations were compared to determine if increased elevation was associated with deterioration in pollinator service. • Key Results In contrast to most heterostylous species, both distylous and homostylous morphs of P. oreodoxa are highly self-compatible, but only homostyles have the facility for autonomous self-pollination. Homostyles set significantly more fruit and seeds following open pollination than the distylous morphs. Visitation by long- tongued pollinators was significantly lower in homostylous populations, and overall rates of insect visitation decreased with elevation. Genetic diversity was significantly lower in homostylous populations, with evidence of increased inbreeding at higher elevation. Patterns of cpDNA variation were consistent with multiple transitions from distyly to homostyly and limited gene flow among populations. • Conclusions The results of this study support the hypothesis that the multiple loss of floral polymorphism in distylous P. oreodoxa is associated with unsatisfactory pollinator service, with homostyles benefiting from reproductive assurance as a result of autonomous self-pollination. Key words: Genetic diversity, heterostyly, homostyly, inbreeding, mating systems, Primula, reproductive assurance. INTRODUCTION autonomous self-pollination (Piper et al., 1984; Ganders et al., 1985; Barrett et al., 1989; Belaoussoff and Shore, 1995). In The evolutionary breakdown of heterostyly represents a para- common with mating system transitions in non-heterostylous digmatic model system for studies of reproductive transitions lineages (reviewed in Stebbins, 1974; Levin, 2012; Igic and in flowering plants. In numerous families, the style and stamen Busch, 2013; Wright et al., 2013; Barrett et al., 2014), the shift polymorphisms that comprise the heterostylous syndrome are to selfing can have important influences on the ecology, demog- lost and are replaced by a monomorphic condition referred to raphy, genetics and evolution of populations. Therefore, iden- as homostyly (Darwin, 1877; Baker, 1966; Charlesworth and tifying the environmental conditions favouring transitions to Charlesworth, 1979; Ganders, 1979; Barrett, 1989; Weller, selfing and determining their population genetic consequences 1992; Richards, 1997; Chen et al., 2013). This change in flo- can provide insights into how often and why selfing evolves in ral biology and population morph structure has an important heterostylous lineages. influence on the mating system of populations. Outbreeding in The most widely invoked selective mechanism to explain heterostylous populations is replaced by high levels of self-fer- why selfing evolves from outcrossing is Darwin’s reproductive tilization owing to the capacity of homostyles to set seed from assurance hypothesis (Darwin, 1876). Unsatisfactory pollinator © The Author 2017. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: [email protected] Downloaded from https://academic.oup.com/aob/article-abstract/120/5/775/4159293 by University of Toronto user on 05 December 2017 776 Yuan et al. — Evolution of selfing from outcrossing service and/or a scarcity of mates can result in pollen limita- incompatibility (Darwin, 1862, 1877). Since then, theoretical tion of outcrossed seed set and conditions favouring increased studies (Charlesworth and Charlesworth, 1979) and empirical levels of self-pollination (Eckert et al., 2006; Moeller, 2006; work on the reproductive ecology (Ornduff, 1979; Piper et al., Busch and Delph, 2012). Under persistent outcrossed pollen 1984; Keller et al., 2014), inheritance patterns (Mather, 1950; limitation, floral variants with a well-developed capacity for Dowrick, 1956; Bodmer, 1960), phylogeography (Guggisberg autonomous self-pollination are favoured by fertility selection, et al., 2006; Zhou et al., 2017), systematics and comparative although other potential reproductive options may occur (see biology (Richards, 2003; Mast et al., 2006) and genetic archi- Harder and Aizen, 2010). Identifying the demographic condi- tecture (Hu et al., 2016; Li et al., 2016; Burrows and McCubbin, tions in which selfing is favoured most often focuses on con- 2017) of distyly and homostyly have provided a valuable frame- ditions of low density (allele effects), such as occurs during work for understanding the repeated loss of floral polymorphism colonizing episodes, including island colonization, or in geo- in the genus. Primula is comprised of approx. 430 species of graphically marginal populations (Baker, 1955; Dornier et al., which 95 % are distylous and 45 species are homostylous, with 2008; Levin, 2012; Pannell, 2015). However, insufficient and/or homostyles distributed across 19 of the 38 sections, virtually all inefficient pollinator service resulting in floral mechanisms pro- of which also contain distylous species (Richards, 2003; Mast moting reproductive assurance can also be selected in diverse et al., 2006; de Vos et al., 2014). Phylogenetic reconstructions ecological contexts including tropical forests (Fan et al., 2012), in Primula indicate that homostyly has had multiple independ- deserts (Yin et al., 2016) and alpine environments (de Vos et al., ent origins from distyly in the genus (Mast et al., 2006), and 2012). Investigations of pollinator service along environmental studies on species with intraspecific variation in floral polymor- gradients may be especially useful for examining the ecologi- phism have provided convincing evidence that homostyles in cal context in which mating system transitions occur, although distylous species are evolutionarily derived from heterostylous this has not been examined for the evolutionary breakdown of morphs (Crosby, 1949; Charlesworth and Charlesworth, 1979; heterostyly to homostyly. Zhou et al., 2017). These evolutionary transitions to homostyly The evolution of selfing has profound consequences for represent a remarkable example of the convergent loss of floral the genetic structure of populations, including the amounts polymorphism, raising important questions concerning the eco- and partitioning of genetic diversity within and among popu- logical and genetic mechanisms involved. lations. Inbreeding decreases heterozygosity, and persistent Although the majority of Primula species are either distylous selfing results in populations that are less diverse and more or homostylous, a few are known that are comprised of a mixture differentiated from one another than outcrossing populations of the two floral conditions (Charlesworth and Charlesworth, (Allard et al., 1968; Jain, 1976; Charlesworth and Pannell, 1979; Richards, 1997). For example, in the widespread P. vul- 2001). Increased selfing rates also reduce effective population garis, homostylous plants are reported from two small areas size, causing populations to lose genetic diversity owing to within the UK, where they coexist in populations with disty- stochastic forces including drift and founder events (Wright, lous morphs at varying
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