The Evolution of Recombination under Domestication: A Test of Two Hypotheses

Department of Genetics, Life Sciences Building, University of Georgia, Athens, Georgia, 30602, USA.
The American Naturalist (Impact Factor: 3.83). 02/2004; 163(1):105-12. DOI: 10.1086/380606
Source: PubMed


The successful domestication of wild plants has been one of the most important human accomplishments of the last 10,000 yr. Though our empirical knowledge of the genetic mechanisms of plant domestication is still relatively limited, there exists a large body of theory that offers a host of hypotheses on the genetics of domestication. Two of these that have not been addressed concern the role of recombination in the process of domestication. The first predicts an increase in recombination rate through domestication, while the second argues that recombination rate should serve as a preadaptation to domestication. This study makes use of data on chiasma frequencies available from almost a century of plant cytogenetical literature to test these two hypotheses. The results support the hypothesis that domestication selects for an increase in recombination, and in rejecting the preadaptation hypothesis, they suggest directions for future research into the possibility of preadaptation to domestication.

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Available from: Jeffrey Ross-Ibarra, Feb 19, 2014
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    • "Ever since Darwin, investigations of domesticated plants and animals have made key contributions to the study of evolution; for recent examples, see [76]–[81]. "
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    ABSTRACT: Domestication can influence many functional traits in plants, from overall life-history and growth form to wood density and cell wall ultrastructure. Such changes can increase fitness of the domesticate in agricultural environments but may negatively affect survival in the wild. We studied effects of domestication on stem biomechanics in manioc by comparing domesticated and ancestral wild taxa from two different regions of greater Amazonia. We compared mechanical properties, tissue organisation and wood characteristics including microfibril angles in both wild and domesticated plants, each growing in two different habitats (forest or savannah) and varying in growth form (shrub or liana). Wild taxa grew as shrubs in open savannah but as lianas in overgrown and forested habitats. Growth form plasticity was retained in domesticated manioc. However, stems of the domesticate showed brittle failure. Wild plants differed in mechanical architecture between shrub and liana phenotypes, a difference that diminished between shrubs and lianas of the domesticate. Stems of wild plants were generally stiffer, failed at higher bending stresses and were less prone to brittle fracture compared with shrub and liana phenotypes of the domesticate. Biomechanical differences between stems of wild and domesticated plants were mainly due to changes in wood density and cellulose microfibril angle rather than changes in secondary growth or tissue geometry. Domestication did not significantly modify "large-scale" trait development or growth form plasticity, since both wild and domesticated manioc can develop as shrubs or lianas. However, "finer-scale" developmental traits crucial to mechanical stability and thus ecological success of the plant were significantly modified. This profoundly influenced the likelihood of brittle failure, particularly in long climbing stems, thereby also influencing the survival of the domesticate in natural situations vulnerable to mechanical perturbation. We discuss the different selective pressures that could explain evolutionary modifications of stem biomechanical properties under domestication in manioc.
    PLoS ONE 09/2013; 8(9):e74727. DOI:10.1371/journal.pone.0074727 · 3.23 Impact Factor
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    • "Third, most of the taxa considered in the mammalian analysis were (partially) outbred or domesticated species , whereas the analysis of recombination rate variation among murid rodents presented here relies heavily on estimates obtained from fully inbred animals. Recombination rates commonly increase in response to inbreeding (Burt and Bell 1987; Ross-Ibarra 2004), but a sample of outbred Gough Island mice have recombination rates comparable to, if not slightly higher than, wild-derived inbred strains of M. m. domesticus. In addition, we note that most hybrid F 1 males from intraand inter-subspecific crosses of house mice have recombination rates intermediate between the values for the two parental strains, revealing minimal evidence for inbreeding depression in recombination rate. "
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    ABSTRACT: Although very closely related species can differ in their fine-scale patterns of recombination hotspots, variation in the average genomic recombination rate among recently diverged taxa has rarely been surveyed. We measured recombination rates in eight species that collectively represent several temporal scales of divergence within a single rodent family, Muridae. We used a cytological approach that enables in situ visualization of crossovers at meiosis to quantify recombination rates in multiple males from each rodent group. We uncovered large differences in genomic recombination rate between rodent species, which were independent of karyotypic variation. The divergence in genomic recombination rate that we document is not proportional to DNA sequence divergence, suggesting that recombination has evolved at variable rates along the murid phylogeny. Additionally, we document significant variation in genomic recombination rate both within and between subspecies of house mice. Recombination rates estimated in F(1) hybrids reveal evidence for sex-linked loci contributing to the evolution of recombination in house mice. Our results provide one of the first detailed portraits of genomic-scale recombination rate variation within a single mammalian family and demonstrate that the low recombination rates in laboratory mice and rats reflect a more general reduction in recombination rate across murid rodents.
    Genetics 12/2010; 187(3):643-57. DOI:10.1534/genetics.110.123851 · 5.96 Impact Factor
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    • "Indeed, different ecological and selective patterns might result in altered levels of recombination [6-8]. For example, domesticated plants tend to have higher rates of recombination than their wild ancestors or relatives [7]. Nevertheless, our comparative analyses pointed out that the putative differences between the genome-wide recombination rates of domesticated taxa and their undomesticated relatives were low when they were compared to the differences observed between distantly related species (see Materials & Methods for more details). "
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    ABSTRACT: Despite its role as a generator of haplotypic variation, little is known about how the rates of recombination evolve across taxa. Recombination is a very labile force, susceptible to evolutionary and life trait related processes, which have also been correlated with general levels of genetic diversity. For example, in plants, it has been shown that long-lived outcrossing taxa, such as trees, have higher heterozygosity (He) at SSRs and allozymes than selfing or annual species. However, some of these tree taxa have surprisingly low levels of nucleotide diversity at the DNA sequence level, which points to recombination as a potential generator of genetic diversity in these organisms. In this study, we examine how genome-wide and within-gene rates of recombination evolve across plant taxa, determine whether such rates are influenced by the life-form adopted by species, and evaluate if higher genome-wide rates of recombination translate into higher He values, especially in trees. Estimates of genome-wide (cM/Mb) recombination rates from 81 higher plants showed a significant phylogenetic signal. The use of different comparative phylogenetic models demonstrated that there is a positive correlation between recombination rate and He (0.83 +/- 0.29), and that trees have higher rates of genome-wide recombination than short-lived herbs and shrubs. A significant taxonomic component was further made evident by our models, as conifers exhibited lower recombination rates than angiosperms. This trend was also found at the within-gene level. Altogether, our results illustrate how both common ancestry and life-history traits have to be taken into account for understanding the evolution of genetic diversity and genomic rates of recombination across plant species, and highlight the relevance of species life forms to explain general levels of diversity and recombination.
    BMC Evolutionary Biology 01/2010; 10(1):22. DOI:10.1186/1471-2148-10-22 · 3.37 Impact Factor
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