Cryptic variation between species and the basis of hybrid performance

U. Rosas, N.H. Barton, L. Copsey, P. Barbier De Reuille, E. Coen, PLoS Biology 8 (2010) e1000429.

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Abstract
Crosses between closely related species give two contrasting results. One result is that species hybrids may be inferior to their parents, for example, being less fertile [1]. The other is that F1 hybrids may display superior performance (heterosis), for example with increased vigour [2]. Although various hypotheses have been proposed to account for these two aspects of hybridisation, their biological basis is still poorly understood [3]. To gain further insights into this issue, we analysed the role that variation in gene expression may play. We took a conserved trait, flower asymmetry in Antirrhinum, and determined the extent to which the underlying regulatory genes varied in expression among closely related species. We show that expression of both genes analysed, CYC and RAD, varies significantly between species because of cis-acting differences. By making a quantitative genotype-phenotype map, using a range of mutant alleles, we demonstrate that the species lie on a plateau in gene expression-morphology space, so that the variation has no detectable phenotypic effect. However, phenotypic differences can be revealed by shifting genotypes off the plateau through genetic crosses. Our results can be readily explained if genomes are free to evolve within an effectively neutral zone in gene expression space. The consequences of this drift will be negligible for individual loci, but when multiple loci across the genome are considered, we show that the variation may have significant effects on phenotype and fitness, causing a significant drift load. By considering these consequences for various gene-expression-fitness landscapes, we conclude that F1 hybrids might be expected to show increased performance with regard to conserved traits, such as basic physiology, but reduced performance with regard to others. Thus, our study provides a new way of explaining how various aspects of hybrid performance may arise through natural variation in gene activity.
Publishing Year
Date Published
2010-07-20
Journal Title
PLoS Biology
Acknowledgement
This was supported by a Marie Curie grant for early stage training and the BBSRC-John Innes Centre PhD Rotation Program. We would like to thank X. Feng and A. Hudson for assistance with introgressions and genotyping; A. Green, A. Bangham and J. Pateman for advice and assistance on shape model procedures; F. Alderson and S.Mitchell from JIC horticultural services; P.J. Wittkopp for protocols and advice on pyrosequencing; and R. Sablowski for discussions and comments.
Volume
8
Issue
7
Article Number
e1000429
IST-REx-ID

Cite this

Rosas U, Barton NH, Copsey L, Barbier De Reuille P, Coen E. Cryptic variation between species and the basis of hybrid performance. PLoS Biology. 2010;8(7):e1000429. doi:10.1371/journal.pbio.1000429
Rosas, U., Barton, N. H., Copsey, L., Barbier De Reuille, P., & Coen, E. (2010). Cryptic variation between species and the basis of hybrid performance. PLoS Biology, 8(7), e1000429. https://doi.org/10.1371/journal.pbio.1000429
Rosas, Ulises, Nicholas H Barton, Lucy Copsey, Pierre Barbier De Reuille, and Enrico Coen. “Cryptic Variation between Species and the Basis of Hybrid Performance.” PLoS Biology 8, no. 7 (2010): e1000429. https://doi.org/10.1371/journal.pbio.1000429.
U. Rosas, N. H. Barton, L. Copsey, P. Barbier De Reuille, and E. Coen, “Cryptic variation between species and the basis of hybrid performance,” PLoS Biology, vol. 8, no. 7, p. e1000429, 2010.
Rosas U, Barton NH, Copsey L, Barbier De Reuille P, Coen E. 2010. Cryptic variation between species and the basis of hybrid performance. PLoS Biology. 8(7), e1000429.
Rosas, Ulises, et al. “Cryptic Variation between Species and the Basis of Hybrid Performance.” PLoS Biology, vol. 8, no. 7, Public Library of Science, 2010, p. e1000429, doi:10.1371/journal.pbio.1000429.
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