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

Abstract

Speciation in the ocean could differ from terrestrial environments due to fewer barriers to gene flow. Hence, sympatric speciation might be common, with American and European eel being candidates for exemplifying this. They show disjunct continental distributions on both sides of the Atlantic, but spawn in overlapping regions of the Sargasso Sea from where juveniles are advected to North American, European and North African coasts. Hybridization and introgression are known to occur, with hybrids almost exclusively observed in Iceland. Different speciation scenarios have been suggested, involving either vicariance or sympatric ecological speciation. Using RAD sequencing and whole‐genome sequencing data from parental species and F1 hybrids, we analysed speciation history based on the joint allele frequency spectrum (JAFS) and pairwise sequentially Markovian coalescent (PSMC) plots. JAFS supported a model involving a split without gene flow 150,000–160,000 generations ago, followed by secondary contact 87,000–92,000 generations ago, with 64% of the genome experiencing restricted gene flow. This supports vicariance rather than sympatric speciation, likely associated with Pleistocene glaciation cycles and ocean current changes. Whole‐genome PSMC analysis of F1 hybrids from Iceland suggested divergence 200,000 generations ago and indicated subsequent gene flow rather than strict isolation. Finally, simulations showed that results from both approaches (JAFS and PSMC) were congruent. Hence, there is strong evidence against sympatric speciation in North Atlantic eels. These results reiterate the need for careful consideration of cases of possible sympatric speciation, as even in seemingly barrier‐free oceanic environments palaeoceanographic factors may have promoted vicariance and allopatric speciation.

Assessing Temporal Patterns and Species Composition of Glass Eel (Anguilla spp.) Cohorts in Sumatra and Java Using DNA Barcodes

“…Likewise, mechanisms inducing glass eel migration choices may account for these large differences between glass and yellow/silver eel mitochondrial genetic diversity. Natal homing, that is migration directed towards parental habitats, is currently observed for A. anguilla and A. americana, which seemingly share spawning grounds in the Atlantic Ocean and hybridize but whose yellow/silver eels do not co-occur in Europe and North America [89][90][91]. Alternatively, inter-annual variability in reproductive success and larval survival might be responsible for these large differences between glass and yellow/silver eel genetic diversity in A. marmorata, A. bicolor and A. bengalensis/A.…”

Inferring the Demographic History of Japanese Eel (Anguilla japonica) from Genomic Data: Insights for Conservation and Fisheries Management

“…One previous study also detected evidence of a population bottleneck 3−8 kya (Tseng et al, 2003), a time period not covered by the PSMC or MSMC analyses. Finally, comparison to analyses of population demographic history in other Anguilla species suggest that Japanese eel has always had a relatively lower N e compared to its congeners (Barth et al, 2020;Nikolic et al, 2020). Together, these findings suggest that Japanese eel has a demographic history of population size fluctuations and has experienced population bottleneck events.…”

“…The copyright holder for this preprint this version posted November 22, 2021. ; https://doi.org/10.1101/2021.11.18.468312 doi: bioRxiv preprint always had a relatively lower N e compared to its congeners (Barth et al, 2020;Nikolic et al, 2020). Together, these findings suggest that Japanese eel has a demographic history of population size fluctuations and has experienced population bottleneck events.…”

“…Inferences of past changes in N e were made by utilising whole genome re-sequencing data of Japanese eel from two sources: the previously published data of Igarashi et al, 2018 and new data described here. The results were compared with those from previous studies on Japanese eel using 'traditional' markers (Tseng et al, 2012(Tseng et al, , 2003, as well as with similar analyses in other Anguilla species (Barth et al, 2020;Nikolic et al, 2020), to provide fisheries management agencies with a broader perspective of the current status of Japanese eel populations.…”

“…However, these patterns of demographic history are not evident in all at risk species. For example, species that have experienced recent population declines, such as the commercially exploited fish species European eel (Nikolic et al, 2020), Atlantic cod and haddock (Tørresen et al, 2018), and yellowfin tuna (Barth et al, 2017), all show evidence of historical population size increase leading up until the last glacial maximum (LGM, 19−33 kya;Clark et al, 2009), after which they experienced population bottlenecks. Such bottleneck events may be considered as random catastrophes which can contribute to a species risk of extinction (Lande 1993).…”