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Open Access Research

Non-homogeneous combination of two porous genomes induces complex body shape trajectories in cyprinid hybrids

Melthide Sinama1*, André Gilles1, Caroline Costedoat1, Emmanuel Corse1, Jean-Michel Olivier2, Rémi Chappaz1 and Nicolas Pech1

Author Affiliations

1 Aix-Marseille Université, CNRS, IRD, IMBE – UMR 7263, Equipe Evolution Génome Environnement, Centre Saint-Charles, Case 36, 3 place Victor Hugo, Marseille Cedex 3 13331, France

2 Université Lyon 1, CNRS, UMR 5023 - LEHNA, Laboratoire d'Ecologie des Hydrosystèmes Naturels et Anthropisés Bât. Forel, Villeurbanne Cedex F-69622, France

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Frontiers in Zoology 2013, 10:22  doi:10.1186/1742-9994-10-22

Published: 1 May 2013

Abstract

Introduction

Hybridization is a common phenomenon in fish and is considered to be a major source of diversification. Deciphering the remoulding of genomic regions and phenotypes in zones where hybrid specimens occur is of particular interest to elucidate the emergence of evolutionary novelties. This approach is particularly challenging because the first step of hybridization seems to be the most important stage in the emergence of hybrid lineages. However, the signal can be significantly altered after only a few generations.

Results

We studied 41 microsatellites and partial cytochrome b gene sequences in 970 specimens belonging to two fish species (Chondrostoma nasus and Parachondrostoma toxostoma) in allopatric/parapatric zones, hybrids between them in a natural sympatric zone: the Ardèche basin. We showed that the genomic architecture in hybrids presented pattern heterogeneity of selection for the different loci. Indeed, the upstream part of the river (Rosières and Labeaume) presented an overdominant fitness of heterozygotes (12.20%) corresponding to a genomic compatibility, and underselection was observed for 4.88%-7.32% of the loci tested indicating a genomic incompatibility. Moreover the upstream station (Rosières) presented a positive selection of invasive C. nasus homozygotes (17.07% to 21.95%) indicating that hybridization may increase the fitness of admixed individuals.

We showed that hybrid morphology (body shape based on 21 landmarks) correlated with genomic dilution indicating a species fingerprint. However, we demonstrated that the hybrid morphology was not a linear modification between the two parental species but a trade-off between several correlated traits.

Conclusions

Hybrid specimens present a mosaic of genomic combination, showing regions with genomic compatibility and others with genomic incompatibility between the two species. Positive selection (invasive advantage ranging from 9.76% to 21.95% of the loci) was evidenced in the upstream part of the Ardèche indicating that environmental selection makes a substantial contribution. Although the presence of a dam is known to impose heterogeneous hybrid zones between these two species, we demonstrated in this study that a natural environment can also generate a hybrid zone with a large number (and diversity) of hybrids. The combination of the two genomes in the hybrids results in complex ontogenetic trajectories (with different morphological traits evolving at different rates) that correspond to novel developmental pathways.

Keywords:
Hybridization; Introgression; Mitochondrial DNA; Microsatellites; Transgressive segregation; Ecological cline; Ontogeny; Fish; Invasive species