Convergent evolution of polyploid genomes from across the eukaryotic tree of life

Author:

Hao Yue1ORCID,Fleming Jonathon2,Petterson Joanna3,Lyons Eric4ORCID,Edger Patrick P56,Pires J Chris789ORCID,Thorne Jeffrey L2101112ORCID,Conant Gavin C21012ORCID

Affiliation:

1. Biodesign Center for Mechanisms of Evolution, Arizona State University , Tempe, AZ 85281, USA

2. Bioinformatics Research Center, North Carolina State University , Raleigh, NC 27695, USA

3. Department of Biomedical Engineering, North Carolina State University , Raleigh, NC 27695, USA

4. School of Plant Sciences, University of Arizona , Tucson, AZ 85721, USA

5. Department of Horticulture, Michigan State University , East Lansing, MI 48824, USA

6. Ecology, Evolutionary Biology and Behavior, Michigan State University , East Lansing, MI 48824, USA

7. International Plant Science Center, New York Botanical Garden , Bronx, NY 10458, USA

8. Division of Biological Sciences, University of Missouri , Columbia, MO 65211, USA

9. Bond Life Sciences Center, University of Missouri , Columbia, MO 65211, USA

10. Program in Genetics, North Carolina State University , Raleigh, NC 27695, USA

11. Department of Statistics, North Carolina State University , Raleigh, NC 27695, USA

12. Department of Biological Sciences, North Carolina State University , Raleigh, NC 27695, USA

Abstract

Abstract By modeling the homoeologous gene losses that occurred in 50 genomes deriving from ten distinct polyploidy events, we show that the evolutionary forces acting on polyploids are remarkably similar, regardless of whether they occur in flowering plants, ciliates, fishes, or yeasts. We show that many of the events show a relative rate of duplicate gene loss before the first postpolyploidy speciation that is significantly higher than in later phases of their evolution. The relatively weak selective constraint experienced by the single-copy genes these losses produced leads us to suggest that most of the purely selectively neutral duplicate gene losses occur in the immediate postpolyploid period. Nearly all of the events show strong evidence of biases in the duplicate losses, consistent with them being allopolyploidies, with 2 distinct progenitors contributing to the modern species. We also find ongoing and extensive reciprocal gene losses (alternative losses of duplicated ancestral genes) between these genomes. With the exception of a handful of closely related taxa, all of these polyploid organisms are separated from each other by tens to thousands of reciprocal gene losses. As a result, it is very unlikely that viable diploid hybrid species could form between these taxa, since matings between such hybrids would tend to produce offspring lacking essential genes. It is, therefore, possible that the relatively high frequency of recurrent polyploidies in some lineages may be due to the ability of new polyploidies to bypass reciprocal gene loss barriers.

Funder

U.S. National Science Foundation

U.S. National Institutes of Health

Publisher

Oxford University Press (OUP)

Subject

Genetics (clinical),Genetics,Molecular Biology

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