Novelties in Hybrid Zones: Crossroads between Population Genomic and Ecological Approaches

Abstract

BackgroundInterspecific hybridization is widespread, occurring in a taxonomically diverse array of species. The Cyprinidae family, which displays more than 30% hybridization, is a good candidate for studies of processes underlying isolation and speciation, such as genetic exchange between previously isolated lineages. This is particularly relevant in the case of recent hybridization between an invasive species, Chondrostoma nasus nasus (from Eastern Europe), and C. toxostoma toxostoma (a threatened species endemic to southern France), in which bidirectional introgressive hybridization has been demonstrated.Methodology/Principal FindingsWe studied 128 specimens from reference populations and 1495 hybrid zone specimens (two years of sampling and four stations), using five molecular markers (one mitochondrial gene, four nuclear introns), morphology (meristic and plastic characters) and life history traits (weight, size, coefficient of condition, sex, age, shoaling). We identified 65 hybrid combinations and visualized spatial and temporal changes in composition. The direction of mitochondrial introgression was density-dependent in favor of the rarer species and we demonstrate that the sexual selection hypothesis is a preponderant explanation in the asymmetry of introgression. Despite genomic evolution in the hybrid zone, convergence was observed for body shape and coefficient of condition, indicating changes in foraging behavior with respect to reference populations, reflecting strong environmental pressure.Conclusions/SignificanceThe complex rules of hybrid zone dynamics are established very early in the contact zone. We propose “inheritance from the rare species” as a new evolutionary hypothesis for animal models. The endemic species was not assimilated by the invasive species. Survival rates for this species were highest in the middle of the river (the warmest part) due to a trade-off between food availability and fecundity. The environment-independent hybrid combination may result from nuclear-mitochondrial interactions involving the Tpi1b gene or a gene linked to this gene (Chromosome 16). This genomic region is also responsible for shoaling behavior in Danio rerio and is a promising zone for studies of changes in population dynamics and advances in integrated studies of hybrid zones.

Introgressive hybridization as a promoter of genome reshuffling in natural homoploid fish hybrids (Cyprinidae, Leuciscinae)

“…Similarly, AOL-like morphotypes are strikingly more evident at first sight than PDU-or PPO-like morphotypes, owing to the detection of a corneous lower lip otherwise absent in Achondrostoma sp. These results seem conflicting with previous works on hybridizing cyprinids where distinct HZs represented different outcomes of independent hybridization processes (Costedoat et al, 2007;Aboim et al, 2010;Broughton et al, 2011), which means that either the environmental pressure is identical in the HZs considered here (unlikely) or that the endogenous (genetic) selection forces are in fact the strongest in action.…”

“…The extent of hybridization Hybridization may have multiple effects at different stages and spatial contexts (Gerber et al, 2001;Costedoat et al, 2007;Broughton et al, 2011;Abbott et al, 2013). The already surveyed HZs of AOL Â PDU seem to behave differently (Aboim et al, 2010) with character displacement happening towards one or the other parental species (Collares- Pereira and Coelho, 1983;Gante et al, 2004;Aboim et al, 2010).…”

“…In this case study, ecological barriers between hybrids and parental species might be altered and/or degraded, so that gene flow back to pure species never actually ceases. However, the ultimate consequences of such apparently extensive and recurrent events to these populations and species remain unknown, and the probability of fixation of the resulting rearrangements depends on the demography of the hybrid swarms (Gerber et al, 2001;Seehausen, 2004;Costedoat et al, 2007;Broughton et al, 2011;Abbott et al, 2013). Usually disregarded (reviewed in Costedoat et al, 2007), these interactions might ultimately result in speciation or extinction faster than expected.…”

“…However, the ultimate consequences of such apparently extensive and recurrent events to these populations and species remain unknown, and the probability of fixation of the resulting rearrangements depends on the demography of the hybrid swarms (Gerber et al, 2001;Seehausen, 2004;Costedoat et al, 2007;Broughton et al, 2011;Abbott et al, 2013). Usually disregarded (reviewed in Costedoat et al, 2007), these interactions might ultimately result in speciation or extinction faster than expected. Coupling the study of these hybrid complexes with modern genome-wide approaches (Twyford and Ennos, 2012) will allow for the exploration of evolutionarily relevant processes and answering questions inherent to hybridization, its causes, dynamics and impacts.…”

“…Natural introgression is commonly found among freshwater fishes, particularly in Cyprinidae (Scribner et al, 2001), where several cases have been comprehensively evaluated (Gerber et al, 2001;Costedoat et al, 2007;Aboim et al, 2010;Broughton et al, 2011). The different outcomes witnessed (reviewed in Abbott et al, 2013) reinforce the opportunity of using cyprinid fish to search for genomic signatures of hybridization.…”