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Genetic Structure of Dioecious and Trioecious Salix Myrsinifolia Populations at the Border of Geographic Range

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Genetic Structure of Dioecious and Trioecious Salix Myrsinifolia Populations at the Border of Geographic Range Tree Genetics & Genomes (2017) 13:15 DOI 10.1007/s11295-016-1096-6 ORIGINAL ARTICLE Genetic structure of dioecious and trioecious Salix myrsinifolia populations at the border of geographic range P. Mirski1 & E. Brzosko1 & I. Jędrzejczyk2 & J. Kotowicz3 & B. Ostrowiecka1 & A. Wróblewska1 Received: 22 July 2016 /Revised: 16 November 2016 /Accepted: 20 December 2016 # The Author(s) 2017. This article is published with open access at Springerlink.com Abstract Gene flow in plant populations is heavily affected haplotype. This frequency significantly decreased with lati- by species sexual systems. In order to study the effect of sex- tude towards the expansion front. We suspect that the presence ual systems on genetic structure, we examined plastid and of hermaphrodites in trioecious populations may represent a nuclear DNA of 12 dioecious (males and females) and 18 trade-off between the possibility of producing progeny by trioecious (males, females and hermaphrodites) populations single hermaphrodites and genetic variability loss through au- of Salix myrsinifolia—a boreal shrub with slow range expan- togamy. S. myrsinifolia benefits from trioecious sexual sys- sion. Populations were located along latitudinal gradients tems under colonization events. This phenomenon is no lon- across submarginal and marginal parts of the range. ger a gain closer to the core of the species range. Individuals of each sex morph were all hexaploid. We identi- fied 10 chloroplast DNA haplotypes and scored 205 polymor- Keywords Sex structure . Trioecy . Dioecy . Subdioecy . phic bands with amplified fragment length polymorphism. We AFLP found dioecious populations that differed from trioecious pop- ulations via the presence of four unique haplotypes and sig- nificant difference in Nei’s gene diversity index (0.119 vs. Introduction 0.116) and down-weighed marker value (1.17 vs. 1.02). The latter parameter, together with haplotype and nucleotide diver- Patterns of species’ geographic range and genetic diversity are sity, significantly decreased with latitude similar to the expan- strictly shaped by life history traits such as reproduction type, sion front. Also, we found that 89% of hermaphrodite individ- breeding system(s) and dispersal mechanisms as well as nat- uals belong to one distinct in tree parsimony network ural processes or human impacts (e.g. isolation, fragmenta- tion, climate changes) (Hamrick and Godt 1996; Barrett and Communicated by Pär Ingvarsson Husband 1990; Gitzendanner and Soltis 2000;Nybom2004). In order to disperse, species harness evolutionary potential Electronic supplementary material The online version of this article (doi:10.1007/s11295-016-1096-6) contains supplementary material, and adopt various strategies enabling survival, reproduction which is available to authorized users. and geographic expansion. Phenotypic variation positively affects adaptive potential of expanding species and the source * P. Mirski of this plasticity lays in genetic variation. Different patterns of [email protected] genetic variation during range expansion can be found both in theoretical assumptions and experimental studies. In a com- 1 Plant Ecology Department, Institute of Biology, University of prehensive review (134 studies and 115 species), Eckert et al. Białystok, Ciołkowskiego 1J, 15-245 Białystok, Poland (2008) detected a decrease in genetic diversity in 64.2% of 2 Laboratory of Molecular Biology and Cytometry, Department of species. There was an increase in genetic differentiation in Plant Genetics, Physiology and Biotechnology, UTP University of 70.2%. During human-mediated introductions, newly Science and Technology, Kaliskiego 7, 85-796 Bydgoszcz, Poland established populations most often suffered losses of allelic 3 Faculty of Mathematics and Informatics, Univeristy of Białystok, richness and heterozygosity, but rarely also underwent signif- Ciołkowskiego 1M, 15-245 Białystok, Poland icant increase in both parameters (Dlugosch and Parker 2008). 15 Page 2 of 16 Tree Genetics & Genomes (2017) 13:15 Recently, more attention has been paid to the consequences of outcrossing during their lifetime or can wait out unfavourable natural, contemporary range expansions (Banks et al. 2010; conditions. This assumption is supported by high ratio of di- Garroway et al. 2011;Swaegersetal.2013). These studies oecy in trees (i.e. van Dulmen 2001;Gross2005)comparing showed that the current range expansion may not only gener- to other angiosperms (Renner 2014). Thus, we suspect that ate more independently replicated edge populations but also departure from dioecy may be induced in woody species by likely results in different population genetic patterns through- other benefits during colonization phase. The most important out the expansion front. Those differences may derive from benefit is availability of uniparental reproduction (selfing), but population-specific features. there is also a higher probability of cross-pollination and In plants, one species may be characterized by different higher fruit sets. sexual systems. Sex determines the gene flow direction and Obbard et al. (2006) conducted a unique study on the rela- rate. In this context, an interesting and poorly studied problem tion between polygamic sexual system and genetic diversity is the relationship between genetic diversity and phylogeo- patterns in the annual plant Mercurialis annua.Thisspansa graphic patterns of plants characterized by different sexual range of systems from self-compatible monoecy through systems—especially in the course of expansion to new terri- androdioecy to dioecy. The authors assumed that monoecy tories. In plant species characterized by polymorphic sex, we would be favoured during colonization, dioecy under stable expect spatial separation of two or three sex morphs. Apart conditions and androdioecy in intermediate ones. They from well-known dioecy, females and/or males may persist showed that monoecious populations of this species displayed with hermaphrodites in either gynodioecious (pistillate and lower within-population genetic diversity than androdioecious perfect flowers on different plants), androdioecious (staminate populations and higher genetic differentiation than dioecious and perfect flowers on different plants) and/or trioecious (sta- and androdioecious populations. This fits the assumption on minate, pistillate and perfect flowers) populations, respective- the ‘colonization’ role in monomorphic individuals in plants ly (Sakai and Weller 1999). capable of reproduction via different sexual systems. In turn, In dioecious populations, the two sexes are separated fully Dorken et al. (2002) showed a slightly lower (but not statisti- into male and female individuals, and cross-pollination is the cally significant) genetic variation between monoecious and only possible option (Vamosi et al. 2003). In other polymor- dioecious Sagittaria latifolia populations. The substantial phic sexual systems, both obligate outcrossing (females) and levels of selfing and inbreeding depression were expected in mixed mating (hermaphrodites) may occur. In plant species, monoecious species but not dioecious ones. They proposed sexual systems affect their ability to establish new popula- that sexual systems were maintained as the result of habitat tions. In the case of dioecy, females and males may be less differentiation and life history strategy. likely to colonize unoccupied habitat than plants from her- The phylogeographic studies of plant species that exhibit maphroditic populations. This often requires only one individ- variation in sexual systems are extremely scarce, but they ual to establish new populations (Pannell and Barrett 1998). explain the important way in which evolution of plant poly- This concept was already given by Baker (1955, 1967), who morphic sexual systems relates to patterns of colonization and stated that under long-distance dispersal, self-compatible indi- extinction in the metapopulation sense (Dorken and Barrett viduals are more likely to establish new populations than self- 2004; Alonso and Herrera 2011). These authors stressed the incompatible ones (so-called Baker’s law). This law can be origin of a given sexual reproductive system. For example, extrapolated to the general context of colonization events dioecy could be a result of historical factors and could be (Pannell and Barrett 1998). evolved from monoecy (Dorken and Barrett 2004; Panell Importantly, sexual systems influence the genetic diversity and Dorken 2006). Similarly, hermaphroditism emerged as at the population and species level (Dorken et al. 2002; the most likely condition from gynodioecy during two events Obbard et al. 2006;Korbeckaetal.2011). In entomogamous, (Alonso and Herrera 2011). Furthermore, these studies, simi- hermaphroditic colonizers, the founding individuals are often lar to Obbard et al. (2006), unravelled the metapopulation isolated by space and pollinators (avoiding small and sparse hypothesis for the distribution of sexual system. plant populations). This could also favour uniparental repro- Trioecy has received scant attention in population biology duction (Barrett et al. 2008). Such possibility enables popula- and genetic diversity studies because of its rarity in nature tion development, but at the cost of inbreeding. Indeed, genet- (3.6% of flowering plant species, Richards 1997;Albert ic variation is most often reduced, i.e. in introduced vs. native et al. 2013) as well as difficulties with its identification and parts of the range (Kliber and Eckert
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