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

Städler, Thomas; Roselius, Kerstin; Stephan, Wolfgang

doi:10.1111/j.0014-3820.2005.tb01777.x

Cited by 44 publications

(29 citation statements)

References 72 publications

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“…Following the approach pioneered by the authors of the MIMAR software, we developed methods to tackle two limitations of existing estimation procedures: the pervasive problem of intra-locus recombination and the often limited number of loci sequenced (around 10) and individuals sampled. These two factors typically represent severe limitations for studying recent speciation in non-model species, such as wild tomatoes [6], [23].…”

Section: Discussionmentioning

confidence: 99%

“…A second scenario considers divergence with continuing gene flow between populations, for example when species ranges abut (parapatry) or overlap following secondary contact, allowing for introgression. The latter model has been suggested to describe speciation events between human populations and ape species or sub-species [4], Drosophila species [5], and the wild tomato species Solanum peruvianum and S. chilense [6]. Key theoretical predictions have been generated to distinguish parapatric and allopatric population divergence based on genomic data [5], [7].…”

Section: Introductionmentioning

confidence: 99%

“…Not only do these species appear to have recently diverged but gene flow may be on-going [6], [23]. The programs IM, IMa and IMa2 cannot be used due to high levels of intra-locus recombination.…”

Section: Introductionmentioning

confidence: 99%

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Estimating Parameters of Speciation Models Based on Refined Summaries of the Joint Site-Frequency Spectrum

et al. 2011

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Understanding the processes and conditions under which populations diverge to give rise to distinct species is a central question in evolutionary biology. Since recently diverged populations have high levels of shared polymorphisms, it is challenging to distinguish between recent divergence with no (or very low) inter-population gene flow and older splitting events with subsequent gene flow. Recently published methods to infer speciation parameters under the isolation-migration framework are based on summarizing polymorphism data at multiple loci in two species using the joint site-frequency spectrum (JSFS). We have developed two improvements of these methods based on a more extensive use of the JSFS classes of polymorphisms for species with high intra-locus recombination rates. First, using a likelihood based method, we demonstrate that taking into account low-frequency polymorphisms shared between species significantly improves the joint estimation of the divergence time and gene flow between species. Second, we introduce a local linear regression algorithm that considerably reduces the computational time and allows for the estimation of unequal rates of gene flow between species. We also investigate which summary statistics from the JSFS allow the greatest estimation accuracy for divergence time and migration rates for low (around 10) and high (around 100) numbers of loci. Focusing on cases with low numbers of loci and high intra-locus recombination rates we show that our methods for the estimation of divergence time and migration rates are more precise than existing approaches.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Estimating Parameters of Speciation Models Based on Refined Summaries of the Joint Site-Frequency Spectrum

et al. 2011

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“…Since this species harbors the greatest variation of all species in the clade of Lycopersicon , it is an ideal starting point to understand the interplay of functional diversity and natural selection. S. peruvianum diverged from its closest relatives at least 500,000 years ago [31], [32]. Adaptation to biotic factors plays an important role in evolution of this species [30], [33]–[35].…”

Section: Introductionmentioning

confidence: 99%

Balancing Selection at the Tomato RCR3 Guardee Gene Family Maintains Variation in Strength of Pathogen Defense

et al. 2012

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Coevolution between hosts and pathogens is thought to occur between interacting molecules of both species. This results in the maintenance of genetic diversity at pathogen antigens (or so-called effectors) and host resistance genes such as the major histocompatibility complex (MHC) in mammals or resistance (R) genes in plants. In plant–pathogen interactions, the current paradigm posits that a specific defense response is activated upon recognition of pathogen effectors via interaction with their corresponding R proteins. According to the “Guard-Hypothesis,” R proteins (the “guards”) can sense modification of target molecules in the host (the “guardees”) by pathogen effectors and subsequently trigger the defense response. Multiple studies have reported high genetic diversity at R genes maintained by balancing selection. In contrast, little is known about the evolutionary mechanisms shaping the guardee, which may be subject to contrasting evolutionary forces. Here we show that the evolution of the guardee RCR3 is characterized by gene duplication, frequent gene conversion, and balancing selection in the wild tomato species Solanum peruvianum. Investigating the functional characteristics of 54 natural variants through in vitro and in planta assays, we detected differences in recognition of the pathogen effector through interaction with the guardee, as well as substantial variation in the strength of the defense response. This variation is maintained by balancing selection at each copy of the RCR3 gene. Our analyses pinpoint three amino acid polymorphisms with key functional consequences for the coevolution between the guardee (RCR3) and its guard (Cf-2). We conclude that, in addition to coevolution at the “guardee-effector” interface for pathogen recognition, natural selection acts on the “guard-guardee” interface. Guardee evolution may be governed by a counterbalance between improved activation in the presence and prevention of auto-immune responses in the absence of the corresponding pathogen.

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“…Wild Solanum species are in general particularly good model species to study between and within species variation, because they occur in diverse geographic and climatic habitats and have a very well studied demography and known evolutionary history (Städler, Roselius & Stephan, 2005; Städler, Arunyawat & Stephan, 2008; Tellier et al, 2011). Additionally, several studies exist suggesting that bacterial resistance-associated genes are under selective pressure (Rose et al, 2005; Rose et al, 2011; Rose, Michelmore & Langley, 2007).…”

Section: Introductionmentioning

confidence: 99%

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

Stam

Scheikl

Tellier

2017

PeerJ

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Wild tomatoes are a valuable source of disease resistance germplasm for tomato (Solanum lycopersicum) breeders. Many species are known to possess a certain degree of resistance against certain pathogens; however, evolution of resistance traits is yet poorly understood. For some species, like Solanum chilense, both differences in habitat and within species genetic diversity are very large. Here we aim to investigate the occurrence of spatially heterogeneous coevolutionary pressures between populations of S. chilense. We investigate the phenotypic differences in disease resistance within S. chilense against three common tomato pathogens (Alternaria solani, Phytophthora infestans and a Fusarium sp.) and confirm high degrees of variability in resistance properties between selected populations. Using generalised linear mixed models, we show that disease resistance does not follow the known demographic patterns of the species. Models with up to five available climatic and geographic variables are required to best describe resistance differences, confirming the complexity of factors involved in local resistance variation. We confirm that within S. chilense, resistance properties against various pathogens show a mosaic pattern and do not follow environmental patterns, indicating the strength of local pathogen pressures. Our study can form the basis for further investigations of the genetic traits involved.

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

Cited by 44 publications

References 72 publications

Estimating Parameters of Speciation Models Based on Refined Summaries of the Joint Site-Frequency Spectrum

Estimating Parameters of Speciation Models Based on Refined Summaries of the Joint Site-Frequency Spectrum

Balancing Selection at the Tomato RCR3 Guardee Gene Family Maintains Variation in Strength of Pathogen Defense

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

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