Asymmetrical Gene Flow in a Hybrid Zone of Hawaiian Schiedea (Caryophyllaceae) Species with Contrasting Mating Systems

Abstract

Asymmetrical gene flow, which has frequently been documented in naturally occurring hybrid zones, can result from various genetic and demographic factors. Understanding these factors is important for determining the ecological conditions that permitted hybridization and the evolutionary potential inherent in hybrids. Here, we characterized morphological, nuclear, and chloroplast variation in a putative hybrid zone between Schiedea menziesii and S. salicaria, endemic Hawaiian species with contrasting breeding systems. Schiedea menziesii is hermaphroditic with moderate selfing; S. salicaria is gynodioecious and wind-pollinated, with partially selfing hermaphrodites and largely outcrossed females. We tested three hypotheses: 1) putative hybrids were derived from natural crosses between S. menziesii and S. salicaria, 2) gene flow via pollen is unidirectional from S. salicaria to S. menziesii and 3) in the hybrid zone, traits associated with wind pollination would be favored as a result of pollen-swamping by S. salicaria. Schiedea menziesii and S. salicaria have distinct morphologies and chloroplast genomes but are less differentiated at the nuclear loci. Hybrids are most similar to S. menziesii at chloroplast loci, exhibit nuclear allele frequencies in common with both parental species, and resemble S. salicaria in pollen production and pollen size, traits important to wind pollination. Additionally, unlike S. menziesii, the hybrid zone contains many females, suggesting that the nuclear gene responsible for male sterility in S. salicaria has been transferred to hybrid plants. Continued selection of nuclear genes in the hybrid zone may result in a population that resembles S. salicaria, but retains chloroplast lineage(s) of S. menziesii.

A Bayesian Approach to Inferring Rates of Selfing and Locus-Specific Mutation

“…Our estimate of the uniparental proportion s G [median 0.287, 95% BCI ð0:110; 0:478Þ] is similar to the estimate using all information (YYY in Table 1 Table 1) produces estimates of the selfing rate for which the 95% BCIs exclude zero. This unexpected estimate of RMES stands in opposition to previous work supporting the presence of selfing in this population of S. salicaria (Wallace et al 2011). Figure 10 presents the inferred distribution across individuals of the number of generations since the most recent outcross event T (Equation 15), averaged over posterior uncertainty, using all data (YYY).…”

“…We analyzed genotypes at nine microsatellite loci from 25 S. salicaria individuals collected from west Maui and identified by Wallace et al (2011) as nonhybrids. We use this analysis to illustrate the incorporation of data in addition to the genotypic scores.…”

“…In our analysis of microsatellite data from the killifish K. marmoratus (Mackiewicz et al 2006;Tatarenkov et al 2012), the expanded-likelihood function corresponds to the product of the probability of the genetic data and the probability of the number of males observed among a total number of individuals (Equation 28). In a similar manner, our analysis of the data set from S. salicaria (Wallace et al 2011) uses an extended-likelihood function that models the observed number of females as a binomial random variable (Equation 29), permitting estimation of the frequency of females among reproductives (p f ).…”

“…Application of the method to simulated data sets demonstrates its accuracy in parameter estimation and in assessing uncertainty. We apply the method to microsatellite data from the self-fertilizing killifish Kryptolebias marmoratus (Mackiewicz et al 2006;Tatarenkov et al 2012) and the gynodioecious Hawaiian endemic Schiedea salicaria (Wallace et al 2011) to illustrate the simultaneous inference of various biologically significant aspects of mating systems in nature, including levels of inbreeding depression, population proportions of sexual forms, and effective numbers. …”

Sex-determining chromosomes and sexual dimorphism: insights from genetic mapping of sex expression in a natural hybrid Fragaria × ananassa subsp. cuneifolia

“…Once viewed as 'evolutionary noise' (Wagner, 1970), hybrid zones are now being viewed as natural laboratories for ecological and evolutionary studies in speciation and diversification (for example, Rieseberg and Wendel, 1993;Sweigart, 2009) as they provide insight into the prevailing direction of gene flow, gene introgression and adaptation (for example, Nolte et al, 2009;Wallace et al, 2011). It also has been noted that natural hybrid zones are an underexploited source of information on reproductive isolation and mating (reviewed in Rieseberg and Blackman, 2010), early sex chromosome evolution (Veltsos et al, 2008) and the genetics of sexual dimorphism (Coyne et al, 2008).…”