Migratory Characteristics as a Key Factor for Determining the Population Structure of a Diadromous Species: Eels Tend to Be Panmictic while Salmon Divide Populations with Ease
Yuki Minegishi, Jun Aoyama, and Katsumi Tsukamoto
Eels and salmon are typical representative fishes of the diadromous life histories of catadromy and anadromy, respectively. Although the population structure of anadromous salmonid species has been well studied, those of catadromous anguillid eels, especially tropical species, are poorly known.
Anguillid eel population structures have been thought to be basically panmictic because they have species-specific spawning areas far offshore and the glass eels recruit randomly to freshwater habitats. However, we found multiple population structures for three anguillid species—giant mottled eel Anguilla marmorata, A. bicolor, and A. australis—by analyzing genetic variations of microsatellite (nuclear DNA) and control region sequences (mitochondrial DNA). Marbled eel has the widest geographic distribution among anguillid species, ranging from the western Indian Ocean to the eastern Pacific Ocean. The analyses for marbled eel (N = 449 individuals) showed significant differences (FST = 0.013–0.240 for microsatellite, 0.053–0.698 for the control region, P < 0.05) among 13 localities throughout their geographic range in different oceans (Madagascar, Réunion, Sumatra, Sulawesi, Philippines, Taiwan, Japan, Guam, Ambon, Papua New Guinea, New Caledonia, Fiji, and Tahiti), whereas no significant differences were observed among localities within the same ocean except for a few comparisons: Papua New Guinea and Tahiti in the South Pacific Ocean for microsatellite (FST = 0.020, P < 0.05), and Sumatra and Réunion in the Indian Ocean for the control region (FST = 0.563, P < 0.001). Large geographic groups were roughly clustered in the neighbor-joining tree based on the control region. We suggest that marbled eel was composed of four genetically different populations: North Pacific, South Pacific, Indian Ocean, and Mariana (Figure 1). Each population was considered to be fully panmictic or to have a totally connected metapopulation structure (Minegishi et al. 2008).
Anguilla bicolor and A. australis (Minegishi et al. 2008) have been classified as two subspecies based on their morphological differences, but this classification has been debated recently. Their subspecies have been described as A. bicolor bicolor in the Indian Ocean, A. bicolor pacifica in the Pacific Ocean, A. australis australis in Australia, and A. australis schmidtii in New Zealand. Our study revealed that A. bicolor (N = 145), from six representative localities in their species range (Madagascar, Réunion, Seychelles, Mayotte, Sumatra, and Philippines), showed clear divergence between the Indian Ocean (A. bicolor bicolor) and Pacific Ocean (A. bicolor pacifica) (FST= 0.018 and 0.697–0.706, P < 0.001). Anguilla australis (N = 73) from Australia and New Zealand showed slight but statistically significant differences (FST = 0.019 and 0.037, P < 0.001). These results support the subspecies designations that have long been accepted.
The population structure of anguillid eels found in our study corresponds to oceanic scales, and each population shows high genetic homogeneity despite their geographic distributions, ranging over thousands of kilometers. This suggests that they have unique migratory characteristics, such as spawning areas, migratory routes, or spawning periods, that differ from other populations.