Genealogical Footprints of Speciation Processes in Wild Tomatoes: Demography and Evidence for Historical Gene Flow

Abstract

Multilocus studies assessing patterns of nucleotide polymorphism within and among closely related species provide access to genealogical information bearing on demographic and geographic aspects of their speciation history. However, the technical difficulties in obtaining sufficient sequence data have severely limited this approach thus far, especially in outbred plant taxa. We employ the analytical framework of divergence population genetics in testing the isolation model of speciation in three self-incompatible species of wild tomatoes (clade Lycopersicon), in particular the assumption of divergence without gene flow. Based on DNA sequence data for 13 nuclear loci, average levels of silent polymorphism vary more than three-fold among species. We estimate a large effective population size for the ancestral species, quite similar to that of the highly polymorphic L. peruvianum. The other two species, however, exhibit concordant signatures of population-size reduction. These demographic inferences are biologically plausible and consistent with results obtained from standard neutrality tests. While the isolation model cannot be rejected by goodness-of-fit criteria, patterns of intragenic linkage disequilibrium in L. peruvianum are indicative of historical introgression at least in some regions of the genome. Considered jointly with the geographic pattern of postzygotic reproductive isolation, our results suggest that speciation occurred under residual gene flow, implying natural selection as one of the evolutionary forces driving the diversification of tomato lineages.

Fitness effects of derived deleterious mutations in four closely related wild tomato species with spatial structure

“…For heterozygotes, a dual approach of both cloning before sequencing and direct sequencing was used to obtain the sequences of both alleles. As before, we developed a series of allelespecific sequencing primers whose 3 0 -end was anchored on identified SNPs or indels (for details of this approach, see Städler et al, 2005). Haplotype phase was thus completely resolved for all sequences.…”

“…In addition, this study also analyzes our previously published sequences sampled from each of four populations in both S. peruvianum and S. chilense, as well as outgroup sequences from tomato relatives (Baudry et al, 2001;Roselius et al, 2005;Arunyawat et al, 2007). We also included one previously sequenced sample of S. habrochaites, which was obtained from the Tomato Genetics Resource Center at UC Davis (http://tgrc.ucdavis.edu; accession LA1775, 'Ancash', see Supplementary Table S1 and Städler et al, 2005).…”

Functional gametophytic self-incompatibility in a peripheral population of Solanum peruvianum (Solanaceae)

“…Similar allele pairs across species could be a result of recently shared evolutionary history (Lu, 2001;Sutherland et al, 2008) or introgression among species (for example, Castric et al, 2008). Solanum peruvianum and S. chilense are certainly recently diverged (p0.55 million years, Städler et al, 2008), and analyses of multilocus sequence data suggest historical introgression (Städler et al, 2005(Städler et al, , 2008. Castric et al, 2008 reported sets of similar alleles at the SRK (S-locus receptor kinase) pistil SI specificity determining gene in Arabidopsis lyrata and A. halleri (Brassicaceae) and demonstrated that levels of introgression at SRK were higher than background levels.…”

Multilocus sequence data reveal extensive departures from equilibrium in domesticated tomato (Solanum lycopersicum L.)

“…Self-incompatible (SI) wild tomato species yielded higher estimates of diversity, for example, Solanum habrochaites S Knaap and DM Spooner (one accession), Solanum chilense (Dunal) Reiche (four populations) and S. peruvianum (four populations). Differences observed among wild tomato species in mean diversity have arisen through a variety of factors including mating system, demography and population structure (Baudry et al, 2001;Roselius et al, 2005;Städler et al, 2005;Arunyawat et al, 2007).…”

“…Historical or recent gene flow among wild tomato species (Nesbitt and Tanksley, 2002;Städler et al, 2005;Arunyawat et al, 2007) and between wild species and the cultivar imposes challenges for evolutionary studies. Notably, a Mexican versus a South American domestication origin continues to be debated Peralta and Spooner, 2007).…”