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Monolithic sandstone continental islands of northern Australia unlock secrets of breeding system evolution in five sympatrically occurring species of the Australian spiny Solanum (Solanaceae) lineage Actions

Topic: Monolithic sandstone continental islands of northern Australia unlock secrets of breeding system evolution in five sympatrically occurring species of the Australian spiny Solanum (Solanaceae) lineage
Presenter: Jason Cantley

While functional dioecy is rare in the genus Solanum (Solanaceae), a relatively high concentration of species (around 20) with the condition occur in northern Australia. These taxa, all members of the “spiny solanums” (Solanum subgenus Leptostemonum), are associated with large sandstone monoliths/escarpments, with populations effectively isolated by vast swaths of uninhabited arid lands. Dioecy appears to be a recently evolved breeding system in Australian Solanum and it has been hypothesized that its geographic prevalence was a response to selective pressure towards obligate outcrossing to increase genetic diversity in insular habitats. Other Solanum subg. Leptostemonum taxa occur sympatrically and fundamentally differ only in population size, in breeding systems that allow for the ability to reproduce via self-fertilization (either a hermaphroditic or andromonoecious breeding system), and the ability to produce clones through underground rhizomes. We used these comparable breeding systems as a model system to assess how population genetics are differentially maintained among 20 populations of five taxa representing three sympatric breeding systems using ddRADtag protocols, Illumina sequencing, and the STACKS pipeline. Demographic histories via Extended Bayesian Skyline Plots were used to assess past effective breeding size and bottlenecks. Descriptive statistics plus admixture bar plots suggest dioecious taxa have the highest amount of genetic diversity when populations—i.e. the effective breeding size—are large. The one hermaphroditic taxon had the lowest level of observed genetic heterozygosity and heterozygosity was comparably similar for the andromonoecious taxon. However, a dioecious taxon with small population sizes had genetic diversity similar to that of the two self-fertilizing breeding systems. Further consideration reveals that this dioecious taxon has a different demographic history than the other dioecious taxa examined. Moreover, the taxon is further limited in genetic diversity by the ability to easily produce genetically identical clones through underground rhizomes. This study suggests that the evolution of a dioecious breeding system in “spiny solanums” of Australia may represent an adaptive advantage by increasing genetic diversity through the generation of obligately outcrossing lineages. Therefore, dioecy appears to represent an effective mechanism to avoid inbreeding and maintain genetic diversity. However, the evolutionary advantages of dioecy may be rendered null due to a decreased opportunity for gene migration when population sizes fall below a critical threshold, become extremely isolated, or have a strong propensity to generate clonal genets. This information has implications for the future conservation of dioecious solanums in Australia, which are often uncommon or rare.

Keywords: population genetics, Conservation genetics, ddRADtag, Solanaceae, Solanum, dioecy, andromonoecy, Inbreeding, selfing, outcrossing, Australia

Monolithic sandstone continental islands of northern Australia unlock secrets of breeding system evolution in five sympatrically occurring species of the Australian spiny Solanum (Solanaceae) lineage

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