North–South Colonization Associated with Local Adaptation of the Wild Tomato SpeciesSolanum chilense

Abstract

After colonization population sizes may vary across the species range depending on environmental conditions and following colonizations. An interesting question is whether local adaptation occurs more frequently in large ancestral populations or in small derived populations. A higher number of new mutations and a lower effect of genetic drift should favor selection in large populations, whereas small derived populations may require an initial local adaptation event to facilitate the colonization of new habitats. Wild tomatoes are native to a broad range of different habitats characterized by variable abiotic conditions in South America, and represent an ideal system to study this interplay between demography and natural selection. Population genetic analyses and statistical inference of past demography were conducted on pooled-sequencing data from 30 genes (8,080 single nucleotide polymorphisms) from an extensive sampling of 23 Solanum chilense populations over Chile and Peru. We reveal first a north-south colonization associated with relaxed purifying selection in the south as shown by a decrease of genetic variation and an increasing proportion of nonsynonymous polymorphism from north to south, and population substructure with at least four genetic groups. Second, we uncover a dual picture of adaptation consisting of 1) a decreasing proportion of adaptive amino acid substitutions from north to south suggesting that adaptation is favored in large populations, whereas 2) signatures of local adaptation predominantly occur in the smaller populations from the marginal ranges in the south.

The wild tomato speciesSolanum chilenseshows variation in pathogen resistance between geographically distinct populations

“…In addition, there is little to no genetic exchange between some of the southern most populations that are separated by the extremely dry Atacama desert. This leads to the conclusion that S. chilense can be divided in a northern, a central and two southern genotype groups (Böndel et al, 2015). …”

“…A study of the species’ demography found four genetically distinct groups; one in the north of the range, one in the central region and two in the south (one on the coast and one at high altitudes). Interestingly, the two southern groups are, even though geographically close to each other, more related to the central group than to each other, possibly due to the separating effect of the extremely arid Atacama desert (Böndel et al, 2015). In addition, S. chilense shows clear climatic adaptations.…”

“…We selected seven populations that represent three previously described genotype groups from Peru and Chile (Böndel et al, 2015). Two populations originate from the central range (LA1958, LA3111), two from the coastal regions (LA2932, LA4107) and two from the southern mountainous region (LA4117, LA4330).…”

Persistent seed banking as eco‐evolutionary determinant of plant nucleotide diversity: novel population genetics insights

“…Interestingly, as nucleotide diversity is higher under more persistent seed banks, recombination events are also more easily detectable in polymorphism data. The signatures of very high nucleotide diversity and high effective recombination are, for example, observed in Solanum chilense (Böndel et al ., ) and S. peruvianum (Tellier et al ., ) two outcrossing wild tomato sister species from South America with persistent seed banks. As a test for this hypothesis (Table ), I suggest that controlling for the mode of reproduction, populations (species) with more persistent seed banks should exhibit higher effective recombination rate, higher genetic diversity and smaller amount of linkage disequilibrium (LD) per locus.…”

The Fisher-Wright model with deterministic seed bank and selection

“…This rescaling effect on the coalescence of lineages in a population has also important consequences for the statistical inference of past demographic events [35]. In practice this means that the spatial structure of populations and seed bank effects on demography and selection are difficult to disentangle [5]. Nevertheless, Tellier et al [28] could use this rescaled seed bank coalescent model [19] and Approximate Bayesian Computation to infer the germination rate in two wild tomato species Solanum chilense and S. peruvianum from polymorphism data [29].…”