Assessing pre- and post-zygotic barriers between North Atlantic eels (Anguilla anguilla and A. rostrata)

Abstract

Elucidating barriers to gene flow is important for understanding the dynamics of speciation. Here we investigate pre-and post-zygotic mechanisms acting between the two hybridizing species of Atlantic eels: Anguilla anguilla and A. rostrata. Temporally varying hybridization was examined by analyzing 85 species-diagnostic single-nucleotide polymorphisms (SNPs; F ST ⩾ 0.95) in eel larvae sampled in the spawning region in the Sargasso Sea in 2007 (N = 92) and 2014 (N = 460). We further investigated whether genotypes at these SNPs were nonrandomly distributed in post-F1 hybrids, indicating selection. Finally, we sequenced the mitochondrial ATP6 and nuclear ATP5c1 genes in 19 hybrids, identified using SNP and restriction site associated DNA (RAD) sequencing data, to test a previously proposed hypothesis of cytonuclear incompatibility leading to adenosine triphosphate (ATP) synthase dysfunction and selection against hybrids. No F1 hybrids but only later backcrosses were observed in the Sargasso Sea in 2007 and 2014. This suggests that interbreeding between the two species only occurs in some years, possibly controlled by environmental conditions at the spawning grounds, or that interbreeding has diminished through time as a result of a declining number of spawners. Moreover, potential selection was found at the nuclear and the cytonuclear levels. Nonetheless, one glass eel individual showed a mismatch, involving an American ATP6 haplotype and European ATP5c1 alleles. This contradicted the presence of cytonuclear incompatibility but may be explained by that (1) cytonuclear incompatibility is incomplete, (2) selection acts at a later life stage or (3) other genes are important for protein function. In total, the study demonstrates the utility of genomic data when examining pre-and post-zyotic barriers in natural hybrids.

Speciation history of European (Anguilla anguilla) and American eel (A. rostrata), analysed using genomic data

“…Our results clearly suggest that gene flow between the two Atlantic eel species is still ongoing, as also supported by the detection of admixed individuals in both species dating back to several generations post F1 (Albert et al, ; Jacobsen et al, ; Pujolar, Jacobsen, Als, Frydenberg, Magnussen, et al, ; Pujolar, Jacobsen, Als, Frydenberg, Munch, et al, ). Interspecific gene flow resulting from admixture occurs at variable rates across the genome, indicating the presence of genomic regions that are resistant to introgression (Gagnaire et al, ).…”

“…Reproduction of the two species overlaps temporally and spatially within the frontal zone (McCleave et al, ), leaving ample opportunities for hybridization. However, to date most newly hatched larvae sampled in the Sargasso Sea consist of pure genotypes of both species that co‐occur throughout much of the Sargasso Sea, with only small proportions of different backcross categories (Jacobsen et al, ; Pujolar, Jacobsen, Als, Frydenberg, Magnussen, et al, ). No F1 hybrids have been observed in the spawning region among 552 analysed larvae (Jacobsen et al, ).…”

“…However, to date most newly hatched larvae sampled in the Sargasso Sea consist of pure genotypes of both species that co‐occur throughout much of the Sargasso Sea, with only small proportions of different backcross categories (Jacobsen et al, ; Pujolar, Jacobsen, Als, Frydenberg, Magnussen, et al, ). No F1 hybrids have been observed in the spawning region among 552 analysed larvae (Jacobsen et al, ). In continental Europe and North America, a few later‐generation backcrosses have been identified (one out of 225 European eel and one out of 30 American eel; Pujolar, Jacobsen, Als, Frydenberg, Munch, et al, ), whereas in Iceland, it is well established that both F1 hybrids and backcrosses are relatively abundant (up to 10%–15%; Albert, Jónsson, & Bernatchez, ; Avise et al, ; Gagnaire, Albert, Jónsson, & Bernatchez, ; Pujolar, Jacobsen, Als, Frydenberg, Magnussen, et al, ).…”

“…In continental Europe and North America, a few later‐generation backcrosses have been identified (one out of 225 European eel and one out of 30 American eel; Pujolar, Jacobsen, Als, Frydenberg, Munch, et al, ), whereas in Iceland, it is well established that both F1 hybrids and backcrosses are relatively abundant (up to 10%–15%; Albert, Jónsson, & Bernatchez, ; Avise et al, ; Gagnaire, Albert, Jónsson, & Bernatchez, ; Pujolar, Jacobsen, Als, Frydenberg, Magnussen, et al, ). Evidence for asymmetric introgression from American to European eel has been revealed using nuclear markers (Albert et al, ; Gagnaire et al, ; Pujolar, Jacobsen, Als, Frydenberg, Magnussen, et al, ; Wielgoss, Gilabert, Meyer, & Wirth, ), and genome‐wide SNP analysis has shown the presence of admixed individuals among American eel that have a European ancestor tracing back to only 3–6 generations ago (Jacobsen et al, ). The extent to which hybridization provides an effective bridge to interspecific gene flow therefore remains unclear, and so is the degree of reproductive isolation between species.…”

Isolation und Hybridisierung beim Europäischen und Amerikanischen Aal

“…Jacobsen und Mitarbeiter verglichen 85 SNPs (Single Nucleotide Polymorphism) und deren Verteilung bei 92 (im Jahr 2007) beziehungsweise 460 (2014) Weidenblattlarven aus der Sargassosee . Sie fanden keinen einzigen F1‐Hybriden, aber jeweils zwei Hybrid‐Nachkommen.…”