Abstract
The southern Appalachian (SA) is one of the most biodiversity−rich areas in North America and has been considered a refugium for many disjunct plant species, from the last glacial period to the present. Our study focuses on the SA clonal hornwort, Nothoceros aenigmaticus J. C. Villarreal & K. D. McFarland. This hornwort was described from North Carolina and is widespread in the SA, growing on rocks near or submerged in streams in six and one watersheds of the Tennessee (TR) and Alabama (AR) Rivers, respectively. Males and female populations occur in different watersheds, except in the Little Tennessee (TN) River where an isolated male population exists ca. 48 km upstream from the female populations. The sex ratio of 1:0 seems extreme in each population. In this study, we use nuclear and organellar microsatellites from 250 individuals from six watersheds (seven populations) in the SA region and two populations from Mexico (23 individuals). We, then, selected 86 individuals from seven populations and used genotyping by sequencing to sample over 600 bi-allelic markers. Our results suggest that the SA N. aenigmaticus and Mexican plants are a nested within a clade of sexual tropical populations. In the US populations, we confirm an extreme sex ratio and only contiguous US watersheds share genotypes. The phylogenetic analysis of SNP data resolves four clusters: Mexican populations, male plants (Little Pigeon and Pigeon river watersheds) and two clusters of female plants; one from the Little Tennessee and Hiwassee Rivers (TR) and the other from the Ocoee (TR) and Coosa (AR) Rivers. All clusters are highly differentiated (Fst values over 0.9). In addition, our individual assignment analyses and PCAs reflect the phylogenetic results grouping the SA samples in three clades and recovering males and female plants with high genetic differentiation (Fst values between 0.5 and 0.9 using microsatellites and bi-allelic markers). Our results point to Pleistocene events shaping the biogeographical pattern seen in US populations. The extreme sex ratio reflects isolation and highlights the high vulnerability of the populations in the SA.
Highlights
Skewed sex ratios, dioicy and clonality are prominent features of plant reproductive systems with profound implications on the ecology, evolution and survival of the species (Barrett, 2015; Petry et al, 2016; Scott et al, 2018)
The southern Appalachian (SA) N. aenigmaticus is a recent immigrant from sexual tropical populations with an extreme case of spatial separation of sexes (1:0 ratio)
Based on microsatellite and SNP data, some genotypes are shared between contiguous watersheds, and the current genetic diversity of this species is not partitioned by watersheds
Summary
Dioicy and clonality are prominent features of plant reproductive systems with profound implications on the ecology, evolution and survival of the species (Barrett, 2015; Petry et al, 2016; Scott et al, 2018). In genetically determined sexual systems, the theoretical sex ratio is expected to be close to 1:1 (female: male), if we assume a similar cost to the production of male and female individuals (Fisher, 1930; Scott et al, 2018). Sex ratios can be significantly skewed (Bisang and Hedenäs, 2005; Sinclair et al, 2012). 61% of 234 species of angiosperms distributed among 61 families display a male-biased ratio (Field et al, 2013). Most of the species studied display a strong female-biased ratio. In nearly 85% of the 103 moss and liverworts species surveyed (Bisang and Hedenäs, 2005), females outnumbered males in natural populations. The causes and genetic repercussions of such skewed ratios are being explored (Bisang and Hedenäs, 2005; Bisang et al, 2015, 2017; Baughman et al, 2017; Brzyski et al, 2018)
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