We examined reproductive isolating barriers at four postmating stages among 11 species from the morphologically diverse genus Nolana (Solanaceae). At least one stage was positively correlated with both genetic and geographic distance between species.Postzygotic isolation was generally stronger and faster evolving than postmating prezygotic isolation. In addition, there was no evidence for mechanical isolation, or for reproductive character displacement in floral traits that can influence pollinator isolation. For sexually reproducing plants and animals, the origin of new species involves the evolution of reproductive isolating barriers between diverging lineages. Studying these isolating barriers therefore provides insight into the process of speciation (Coyne and Orr 2004). Several approaches have been used to examine the evolution of reproductive isolation within the same closely related group of species, including examining the relative strength of isolating barriers operating at different reproductive or developmental stages among different species pairs, across different degrees of evolutionary divergence, and/or among reciprocal crosses (Coyne and Orr 2004, and see below). These approaches aim to evaluate how rapidly barriers accumulate and which isolating barriers contribute most during initial divergence between lineages, among other questions. In combination, they can provide insight into the evolutionary forces and the genetic mechanisms responsible for the evolution of new, reproductively independent, lineages.First, examining the reproductive compatibility of a single species pair at multiple developmental stages (e.g., premating, postmating prezygotic, and postzygotic) can be used to infer which stages are most effective at reducing current gene flow between these species, and therefore which stages might have been more or less influential during their initial divergence (e.g., Ramsey et al. 2003;Kay 2006;Martin and Willis 2007;Mendelson et al. 2007;Maroja et al. 2009;Dopman et al. 2010). For example, based on the estimated contributions of multiple preand postzygotic reproductive barriers between two monkeyflower sister species, Mimulus lewisii and M. cardinalis (Ramsey et al. 2003), factors acting prior to hybridization (specifically ecogeographic isolation and pollinator isolation) were inferred to be the primary isolating barriers in this system. Data such as these can also suggest the evolutionary forces that are most likely responsible for reducing gene flow between species. For example, estimates of pre-and postzygotic barriers between M. guttatus and M. nasutus (Martin and Willis 2007) revealed that prezygotic barriers contributed most to total isolation, likely as a result of adaptive divergence in mating systems (i.e., shift to self-pollination) and edaphic ecology (i.e., drought avoidance via phenological acceleration).
Molecular mechanisms underlying the transition from genetic self-incompatibility to self-compatibility are well documented, but the evolution of other reproductive trait changes that accompany shifts in reproductive strategy (mating system) remains comparatively under-investigated. A notable exception is the transition from exserted styles to styles with recessed positions relative to the anthers in wild tomatoes (Solanum Section Lycopersicon). This phenotypic change has been previously attributed to a specific mutation in the promoter of a gene that influences style length (style2.1); however, whether this specific regulatory mutation arose concurrently with the transition from long to short styles, and whether it is causally responsible for this phenotypic transition, has been poorly investigated across this group. To address this gap, we assessed 74 accessions (populations) from 13 species for quantitative genetic variation in floral and reproductive traits as well as the presence/absence of deletions at two different locations (StyleD1 and StyleD2) within the regulatory region upstream of style2.1. We confirmed that the putatively causal deletion variant (a 450-bp deletion at StyleD1) arose within self-compatible lineages. However, the variation and history of both StyleD1 and StyleD2 was more complex than previously inferred. In particular, although StyleD1 was statistically associated with differences in style length and stigma exsertion across all species, we found no evidence for this association within two species polymorphic for the StyleD1 mutation. We conclude that the previous association detected between phenotypic and molecular differences is most likely due to a phylogenetic association rather than a causal mechanistic relationship. Phenotypic variation in style length must therefore be due to other unexamined linked variants in the style2.1 regulatory region.
A goal of speciation genetics is to understand how the genetic components underlying interspecific reproductive barriers originate within species. Unilateral incompatibility (UI) is a postmating prezygotic barrier in which pollen rejection in the female reproductive tract (style) occurs in only one direction of an interspecific cross. Natural variation in the strength of UI has been observed among populations within species in the wild tomato clade. In some cases, molecular loci underlying self-incompatibility (SI) are associated with this variation in UI, but the mechanistic connection between these intra- and inter-specific pollen rejection behaviors is poorly understood in most instances. We generated an F2 population between SI and SC genotypes of a single species, Solanum pennellii, to examine the genetic basis of intraspecific variation in UI against other species, and to determine whether loci underlying SI are genetically associated with this variation. We found that F2 individuals vary in the rate at which UI rejection occurs. One large effect QTL detected for this trait co-localized with the SI-determining S-locus. Moreover, individuals that expressed S-RNase—the S-locus protein involved in SI pollen rejection—in their styles had much more rapid UI responses compared with those without S-RNase protein. Our analysis shows that intraspecific variation at mate choice loci—in this case at loci that prevent self-fertilization—can contribute to variation in the expression of interspecific isolation, including postmating prezygotic barriers. Understanding the nature of such intraspecific variation can provide insight into the accumulation of these barriers between diverging lineages.
23A goal of speciation genetics is to understand how the genetic components underlying 24 interspecific reproductive barriers originate within species. Unilateral incompatibility (UI) is a 25 postmating prezygotic barrier in which pollen rejection in the female reproductive tract (style) 26 occurs in only one direction of an interspecific cross. Natural variation in the strength of UI has 27 been observed among populations within species in the wild tomato clade. In some cases, 28 molecular loci underlying self-incompatibility (SI) are associated with this variation in UI, but the 29 mechanistic connection between these intra-and inter-specific pollen rejection behaviors is 30 poorly understood in most instances. We generated an F 2 population between SI and SC 31 genotypes of a single species, Solanum pennellii, to examine the genetic basis of intraspecific 32 variation in the strength of UI against other species, and to determine whether loci underlying 33 SI are genetically associated with this variation. We found that F 2 individuals vary in the rate at 34 which UI rejection occurs. One large effect QTL detected for this trait co-localized with the SI-35 determining S-locus. Moreover, individuals that expressed S-RNase-the S-locus protein 36 involved in SI pollen rejection-in their styles had much more rapid UI responses compared to 37 those without S-RNase protein. Our analysis shows that intraspecific variation at mate choice 38 loci-in this case at loci that prevent self-fertilization-can contribute to variation in the 39 strength of interspecific isolation, including postmating prezygotic barriers. Understanding the 40 nature of such standing variation can provide insight into the accumulation of these barriers 41 between diverging lineages. 42 43 49reproducing organisms-reproductive isolation, among diverging lineages. Accordingly, loci that 50 contribute to this cumulative process between species must first arise within an individual 51 population prior to spreading to other conspecific populations within their own lineage. During 52 this process, populations of a single species are expected to show varying strengths of 53 reproductive isolation against other lineages; that is, there will be intraspecific genetic variation 54 for the magnitude of interspecific reproductive isolation from other lineages. Intraspecific 55 phenotypic variation in the strength of hybrid incompatibility has been observed in many 56 systems including mammals (Good, Handel and Nachman, 2007; Vyskočilová, Pražanová and 57 60 Sweigart, Mason and Willis, 2007). Understanding the nature, origin, and accumulation of this 61 variation, including the underlying molecular genetic variants responsible, can provide insight 62 into the evolutionary dynamics of lineage divergence (Cutter, 2012), including the order in 63 which alleles contributing to interspecific reproductive isolation arise and fix within diverging 64 lineages. 66The genetic basis of intraspecific variation for interspecific barriers has been 67 in...
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