Abstract
Given their diverse mating systems and recent divergence, wild tomatoes (Solanum section Lycopersicon) have become an attractive model system to study ecological divergence, the build-up of reproductive barriers, and the causes and consequences of the breakdown of self-incompatibility. Here we report on a lesser-studied group of species known as the “Arcanum” group, comprising the nominal species Solanum arcanum, Solanum chmielewskii, and Solanum neorickii. The latter two taxa are self-compatible but are thought to self-fertilize at different rates, given their distinct manifestations of the morphological “selfing syndrome.” Based on experimental crossings and transcriptome sequencing of a total of 39 different genotypes from as many accessions representing each species’ geographic range, we provide compelling evidence for deep genealogical divisions within S. arcanum; only the self-incompatible lineage known as “var. marañón” has close genealogical ties to the two self-compatible species. Moreover, there is evidence under multiple inference schemes for different geographic subsets of S. arcanum var. marañón being closest to S. chmielewskii and S. neorickii, respectively. To broadly characterize the population-genomic consequences of these recent mating-system transitions and their associated speciation events, we fit demographic models indicating strong reductions in effective population size, congruent with reduced nucleotide and S-locus diversity in the two independently derived self-compatible species.
Highlights
The causes and consequences of evolutionary transitions in mating systems have played prominent roles in both fundamental and applied research on flowering plants
We extended the seed sequence collection by BLAST-searching the above sequences against GenBank nt restricted to Solanum section Lycopersicon (NCBI: txid49274) with an e-value threshold of 1e-5
Near-complete hybrid seed failure (HSF) characterized crosses between accessions LA0378 and LA1984 and all other tested ARCA, with limited seed viability only observed in ARC-S × “humicho” crosses (Supplementary Figure 2)
Summary
The causes and consequences of evolutionary transitions in mating systems have played prominent roles in both fundamental and applied research on flowering plants. A related issue of high interest to evolutionary biologists is whether a shift in mating system (SI-to-SC) promotes, or even initiates, the evolutionary divergence of two or more independent lineages, eventually resulting in (at least partial) reproductive isolation and speciation (Cutter, 2019) The latter aspect has been thoroughly investigated in the genus Capsella, where the recently diverged self-compatible Capsella rubella was shown to be derived from the obligately outcrossing Capsella grandiflora (Foxe et al, 2009; Guo et al, 2009; Brandvain et al, 2013; Bachmann et al, 2019). The population genomic consequences of such matingsystem transitions, are still under-explored and have only been extensively studied in few cases (Barrett et al, 2014; Laenen et al, 2018; Cutter, 2019)
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