Studies on natural variation in gene expression and its phenotypic effects provide fresh insights into the origins of vigour and sterility in species hybrids

A. C Whibley

A. D Cutter

A. P McGregor

A. S Kondrashov

C Queitsch

C Shindo

C Weight

C. E. L Baxter

C. R Haag

D Luo

E Sucena

Enrico Coen

G Gibson

H Stubbe

H. A Orr

H. J Muller

I Tirosh

J de Meaux

J Milloz

J Werner

J. A Birchler

J. F Crow

J. M Burke

L Galego

L. J Luo

Lucy Copsey

M Kimura

M-A Felix

M-A Félix

M. C Whitlock

M. M. R Costa

Mohamed A. F. Noor

N. B Langlade

N. H Barton

N. M Springer

Nick H. Barton

P. J Wittkopp

Pierre Barbier de Reuille

R Carpenter

R Lande

R. M Graze

S Bensmihen

S Gavrilets

S Gazzani

S Wright

S. B Corley

S. H Rice

S. L Rutherford

T Gubitz

T. G Dobzhansky

U Johanson

Ulises Rosas

W Bateson

W Rothmaler

W. H Press

X Feng

X Zhang

Z Schwarz-Sommer

Z. J Chen

Ã. l Sucena

PLoS Biology

English

PubMed

Rosas Ulises

Barton Nick H.

Copsey Lucy

Barbier de Reuille Pierre

Coen Enrico

Public Library of Science (PLOS)

Cryptic Variation between Species and the Basis of Hybrid Performance

Crossref

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

Nick H Barton

Directory of Open Access Journals

Cryptic variation between species and the basis of hybrid performance.

Rosas, Ulises

Barton, Nicholas H 

Copsey, Lucy

Barbier De Reuille, Pierre

Coen, Enrico

IST Austria: PubRep (Institute of Science and Technology)

Cryptic variation between species and the basis of hybrid performance

Barton, Nicholas H

ISTA Research Explorer (Institute of Science and Technology Austria)

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.</p

Barton, Nick H.

de Reuille, Pierre Barbier

Edinburgh Research Explorer

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Allele-specific assay reveals functional variation in the chalcone synthase promoter of Arabidopsis thaliana that is compatible with neutral evolution.

Allelic variation and heterosis in maize: how do two halves make more than a whole?

Alternative hypotheses of hybrid vigor.

An introduction to population genetics theory.

Analysis of the molecular basis of flowering time variation in Arabidopsis accessions.

Canalization in evolutionary genetics: a stabilizing theory?

Contamination of the genome by very slightly deleterious mutations: why have we not died 100 times over?

Control of organ asymmetry in flowers of Antirrhinum.

Cryptic quantitative evolution of the vulva intercellular signaling network in caenorhabditis.

Divergence of larval morphology between Drosophila sechellia and its sibling species caused by cis-regulatory evolution of ovo/shaven-baby.

Divergence times in Caenorhabditis and Drosophila inferred from direct estimates of the neutral mutation rate.

Diversification and co-option of RADlike genes in the evolution of floral asymmetry.

Evolution of allometry in Antirrhinum.

Evolution of regulatory interactions controlling floral asymmetry.

Evolution through genetically controlled allometry space.

Evolutionary changes in cis and trans gene regulation.

Evolutionary paths underlying flower color variation in antirrhinum.

Fitness landscapes and the origin of species. Princeton & Oxford:

Fixation of new alleles and the extinction of small populations: drift load, beneficial alleles, and sexual selection.

Floral asymmetry involves an interplay between TCP and MYB transcription factors in Antirrhinum.

Floral homeotic mutations produced by transposon-mutagenesis in Antirrhinum majus. Genes Dev 4: 1483–1493. Cryptic Variation and Hybrid Performance PLoS

FRIGIDA-independent variation in flowering time of natural Arabidopsis thaliana accessions.

Genetic load in sexual and asexual diploids: segregation, dominance and genetic Drift.

Genetic loads at a polymorphic locus mantained by frequency depends selection.

Genetics and the Fitness of Hybrids.

Genetics and the origin of species.

Genetik und Zytologie von Antirrhinum L. sect Antirrhinum.

Global analysis of allele-specific expression in Arabidopsis thaliana.

Heredity and variation in modern lights.

Hsp90 as a capacitor for morphological evolution.

Hsp90 as a capacitor of phenotypic variation.

Hudson A

In search of the molecular basis of heterosis.

Intraspecific evolution of the intercellular signaling network underlying a robust developmental system.

Isolating mechanisms, evolution and temperature.

LeafAnalyser: a computational method for rapid and large-scale analyses of leaf shape variation.

Local drift load and the heterosis of interconnected populations.

Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time.

Molecular mechanisms of polyploidy and hybrid vigor.

Morphological evolution through multiple cis-regulatory mutations at a single gene.

Mutational spaces for leaf shape and size.

Numerical recipes in C: the art of scientific computing. Cambridge: Press Syndicate of the University of Cambridge.

Origin of floral asymmetry in Antirrhinum.

Overdominant epistatic loci are the primary genetic basis of inbreeding depression and heterosis in rice. II. Grain yield components.

Regulatory changes underlying expression differences within and between Drosophila species.

Regulatory divergence in Drosophila melanogaster and D. simulans, a genomewide analysis of allele-specific expression.

Regulatory evolution of shavenbaby/ovo underlies multiple cases of morphological parallelism.

Role of DIVARICATA in the control of dorsoventral asymmetry in Antirrhinum flowers.

Role of FRIGIDA and FLOWERING LOCUS C in determining variation in flowering time of Arabidopsis.

Speciation by postzygotic isolation: forces, genes and molecules.

Taxonomische monographie der gattung Antirrhinum.

The distribution of gene frequencies in populations.

The evolution of canalization and the breaking of Von Baer’s laws: modeling the evolution of development with epistasis.

The minimum number of genes contributing to quantitative variation between and within populations.

The role of hybridization in evolution.

Uncovering cryptic genetic variation.

Wagner A

https://figshare.com/articles/Cryptic_Variation_between_Species_and_the_Basis_of_Hybrid_Performance/142602

Cryptic Variation between Species and the Basis of Hybrid Performance

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Public Library of Science (PLOS)

Crossref

Directory of Open Access Journals

IST Austria: PubRep (Institute of Science and Technology)

ISTA Research Explorer (Institute of Science and Technology Austria)

IST Austria: PubRep (Institute of Science and Technology)

Edinburgh Research Explorer

Public Library of Science (PLOS)