Buffering of developmental noise provides a mechanism for heterosis in both polyploid and diploid hybrids

Abstract

Using an abstract computational model of multicellular development, I show that the deleterious effects of gene expression noise on development are heavily buffered by increased ploidy, both from haploid to diploid cells and from diploid to tetraploid ones. Because the development of large multicellular organisms requires at least millions of individual cell divisions and many specifications of cell fate, it is likely impossible for large organisms to sufficiently control expression noise so as to prevent all noise-related errors in fate determination. However, for any given level of noise tolerance, cells of higher ploidy are less likely to suffer fate determination failure, potentially giving an explanation for the preference for larger organisms to have diploid somatic phases. Ploidy, however, is not the only potential mechanism by which differences in noise tolerance might influence hybrid vigor. Diploid hybrids can also display developmental robustness due to the removal of allelic correlations in expression noise. If we flip this perspective, noise-related disruption of development provides a neutral source of inbreeding depression, whereby sequence similarity throughout the genome induces correlated gene expression noise, reducing developmental robustness and pushing diploids back in the direction of haploid developmental fidelity.