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Microsatellite Evidence for Obligate Autogamy, but Abundant Genetic Variation in the Herbaceous Monocarp Lobelia Inflata (Campanulaceae)

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Microsatellite Evidence for Obligate Autogamy, but Abundant Genetic Variation in the Herbaceous Monocarp Lobelia Inflata (Campanulaceae) doi: 10.1111/jeb.12734 Microsatellite evidence for obligate autogamy, but abundant genetic variation in the herbaceous monocarp Lobelia inflata (Campanulaceae) P. W. HUGHES* & A. M. SIMONS† *Max Planck Institute for Plant Breeding Research, Cologne, Germany †Department of Biology, Carleton University, Ottawa, ON, Canada Keywords: Abstract autogamy; Although high levels of self-fertilization (>85%) are not uncommon in nat- lineage selection; ure, organisms reproducing entirely through selfing are extremely rare. Pre- Lobelia inflata; dominant selfers are expected to have low genetic diversity because genetic self-fertilization; variation is distributed among rather than within lineages and is readily lost semelparity. through genetic drift. We examined genetic diversity at 22 microsatellite loci in 105 individuals from a population of the semelparous herb Lobelia inflata L. and found (i) no evidence of heterozygosity through outcrossing, yet (ii) high rates of genetic polymorphism (2–4 alleles per locus). Furthermore, this genetic variation among lineages was associated with phenotypic traits (e.g. flower colour, size at first flower). Coupled with previous work characteriz- ing the fitness consequences of reproductive timing, our results suggest that temporal genotype-by-environment interaction may maintain genetic varia- tion and, because genetic variation occurs only among lineages, this simple system offers a unique opportunity for future tests of this mechanism. ization present in a species with a mixed mating system Introduction (Johnston & Schoen, 1996; Dudash et al., 1997; Crnok- The fitness consequences of self-fertilization (selfing) rak & Barrett, 2002) have been the subject of considerable attention in evo- Although 10–20% of species are predominantly lutionary ecology (Lande & Schemske, 1985; Schemske (>50%) selfing (Barrett, 2002), only a small minority & Lande, 1985; Barrett & Eckert, 1990; Hereford, are highly (>95%) selfing (Wright et al., 2013). In these 2010). Self-fertilization is favoured over outcrossing species, reproductive assurance is cited as the main evo- when fitness gains due to reproductive assurance, lutionary mechanism favouring extreme selfing over a transmission advantage, isolation from maladaptive mixed mating system (Takebayashi & Morrell, 2001; genes, or density-dependent interactions outweigh neg- Wright et al., 2013; Zhang et al., 2014). However, ative effects associated with inbreeding depression or Wright et al. (2013) also note that ‘marker-based esti- gamete discounting (Jain, 1976; Lande & Schemske, mates of self-fertilization rates suggest that very few if 1985; Schemske & Lande, 1985; Barrett & Eckert, 1990; any plant species are completely selfing’ – that is, obli- Goodwillie et al., 2005). Inbreeding depression may gate selfing is extremely rare or unknown in nature. have slight-to-severe fitness consequences and may Extant mating-system models generally assume that – vary in intensity (Eckert & Barrett, 1994; Husband & in the absence of gene flow among lineages within a Schemske, 1996; Willis, 1999; Armbruster & Reed, population – genetic diversity will gradually erode for 2005). The strength of inbreeding depression is several reasons. As the effective population size of self- negatively associated with the proportion of self-fertil- ers is half that of outcrossers, the effects of genetic drift may be strong (Lande & Schemske, 1985; Schemske & Lande, 1985; Jarne & Charlesworth, 1993; Charles- Correspondence: Patrick William Hughes, Max Planck Institute for Plant Breeding Research, Cologne 50829, Germany. worth & Charlesworth, 1995). Alternative alleles are Tel.:+49 1762 7663 089; fax: +49 221 5062 413; e-mail: ‘captured’ within lineages and cannot be recombined; [email protected] thus, both drift and selective purging of deleterious ª 2015 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY. J. EVOL. BIOL. JOURNAL OF EVOLUTIONARY BIOLOGY ª 2015 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY 1 2 P. W. HUGHES AND A. M. SIMONS alleles will result in low genetic diversity (Husband & selection on lineages with distinct phenotypes (Winton Schemske, 1996; Dudash et al., 1997; Crnokrak & et al., 2006; Tatarenkov et al., 2007; Leys et al., 2014). Barrett, 2002). This leads to the speculation that selfing Moreover, models of genetic variation in predominantly may be irreversible and is therefore an ‘evolutionary selfing species have predicted that relatively high levels dead end’ (Darwin, 1877; Schoen & Brown, 1991; Bar- of genetic variation can be maintained by fluctuating rett & Harder, 1996; Takebayashi & Morrell, 2001; Igic selection (Ellner & Sasaki, 1996; Brys et al., 2011). & Busch, 2013) and may explain the rarity of very high Therefore, if – through autogamous self-fertilization – selfing rates in nature. L. inflata forms genetically identical lineages, temporal In a comparison of predominantly inbreeding and out- fluctuations in fitness among reproductive phenotypes breeding plant species, allelic diversity of inbreeders was may preserve the diversity of genetic lineages, and found to be less than half that of outcrossers, although therefore of alleles, through time. For L. inflata, fitness the variance in allelic diversity among selfing popula- variance within populations may be related to flower- tions was higher (Schoen & Brown, 1991). There are also ing phenology and reproductive effort, as abiotic condi- numerous examples of organisms showing lower allelic tions vary over the course of the season (Hughes & diversity in selfing than in outcrossing populations or Simons, 2014a,c). congeners (e.g. Jarne & Charlesworth, 1993; Dudash To date, obligate autogamy in L. inflata has been an et al., 1997). For example, lower genetic diversity has assumption, based only on circumstantial evidence: been observed in highly selfing populations of Arabidopsis anthesis is extremely brief, and fruit development occurs thaliana than in populations with a higher degree of almost immediately after the initiation of flower forma- outcrossing (Abbot & Gomes, 1989). However, high tion (Simons & Johnston, 2000; Hughes & Simons, levels of within-population allelic diversity have also 2014a,c). Moreover, in each flower the short stigma is been found within predominantly selfing populations of completely enclosed by a tube of anthers, and pollen groups including fungi (Winton et al., 2006), legumes does not appear to disperse outside flowers. Given the (Siol et al., 2007), proteaceous trees (Ayre et al., 1994), rarity of complete selfing in nature, in this study we col- ginger (Zhang & Li, 2008), brittle stars (Boissin et al., lected further evidence concerning the true selfing rate 2008), snails (Viard et al., 1996; Trouve et al., 2003) and of L. inflata. We also assessed the phenotypic conse- killifish (Tatarenkov et al., 2007). quences of a high degree of selfing, as this should be There is thus no simple relationship between mating associated with the formation of genetic lineages, and system and intrapopulation genetic diversity, and little that there is substantial variation in key fitness traits – is known about how genetic diversity is maintained in especially flowering phenology – in field populations of highly selfing species, despite the fact that the partition- L. inflata (Simons & Johnston, 2003; Hughes & Simons, ing of genetic variation in species with mixed mating 2014c). Accordingly, we performed two main analyses. systems is an important and well-studied question in First, we assessed the degree of autogamous selfing and evolutionary ecology (Stebbins, 1974; Barrett & Eckert, genetic structure of a wild population of L. inflata using 1990; Holsinger, 1991; Kalisz et al., 2004; Goodwillie microsatellite marker diversity found in specimens sam- et al., 2005). pled from a field site. Second, to determine whether In this study, we determined the selfing rate and genetic lineages were associated with variation in flow- assessed the degree of genetic diversity in the mono- ering phenology, we evaluated the degree of variation carpic herb Lobelia inflata L. (Campanulaceae). Lobelia in phenotype that was associated with variation among inflata has been assumed to be obligately (autoga- genetic lineages. Low levels of heterozygosity in a field mously) self-fertilizing in previous studies; because a population despite high allelic diversity would support closed corolla tube prevents pollen release (and instead the hypothesis that selfing is predominant in L. inflata; deposits it on the stigma of the same flower), it is not the detection of high levels of heterozygosity would clear how outcrossing may occur in this species (Ames, instead be consistent with outcrossing. Results revealing 1901; Simons & Johnston, 2000; Hughes & Simons, abundant genetic variation among completely selfing 2014b,c). However, the distribution of phenotypic vari- lineages would require an explanation. We propose that ation among lineages in L. inflata is suggestive of consistent differences in reproductive trait values among genetic variation (Hughes et al., 2014), despite the fact lineages could be explained by temporally variable selec- that studies of outcrossing congeners show limited alle- tion in which the rank order of genotypic fitness is envi- lic diversity at genotyped loci (Antonelli, 2008; Geleta ronment-dependent. & Bryngelsson, 2012). Self-fertilization may result in multigenerational genetic lineages, as each parent pro- Materials and methods duces homozygous and genotypically identical off- spring. The null expectation in self-perpetuating genetic Source population
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