Phylogeography of Asian sockeye salmon (Oncorhynchus nerka) based on analysis of mtDNA control region polymorphism

Abstract

Analysis of the contemporary geographic distributions of mtDNA haplotypic diversity of sockeye salmon (Oncorhynchus nerka Walbaum) on the Asian part of its range and consideration of possible scenarios for microevolution of the species were performed. In total, 172 specimens of sockeye salmon from different rivers of Kamchatka, Chukotka, north coast of the Sea of Okhotsk, and from the Kuril Islands were analyzed using the entire mtDNA control region (1,010 bp) sequencing. After multiple alignments of the sequences 16 polymorphic sites were identified. Most of substitutions were detected in the first and the last thirds of the D‐loop sequence, as well as one insertion was registered in the poly‐T region. Two mass haplotypes (Hap_1_10T and Hap_2_13T) were revealed; they were present in most samples and differed by three substitutions and two indels. All the sequence variants were distributed among two haplogroups in compliance with the mass haplotypes. The star‐shaped topology of the MST‐tree points to a rapid increase in the diversity of groups, indicating a rapid expansion of the species after its number reducing in the past. The diversity of the first haplogroup was higher, but its main fraction fell on the samples from the middle reach of Kamchatka River, which seems to be a refugium during the Late Pleistocene glaciation. Presence of both haplogroups in most populations in approximately equal proportions indicates that the entire Asian part of the sockeye salmon range is a zone of secondary contact. We hypothesize that Hap_2_13T had more ancient origin and the Hap_1_10T was formed somewhat later, apparently in Asia, because almost all transitional forms between the haplogroups were found in Iturup Island populations.

Adaptive and Neutral Polymorphisms of the Onne-DAB Gene from the Major Histocompatibility Complex (MHC) in Sockeye Salmon Populations on the Asian Range

“…One of them is believed to be the paleobasin located in the middle sections of the Kamchatka River. Additionally, there is partial evidence indicating a northern origin, likely stemming from the Beringia refugium [61][62][63]. The tendencies of changes in the intrapopulation diversity indices in both loci and in allele frequencies, at least in the intronic MHC2_251v2 locus in the study area (with a number of exceptions), are quite consistent with the prevailing ideas about the formation of the range of this species in Asia.…”

“…Patterns of postglacial sockeye salmon colonization of the Asian coast during the late Pleistocene may be reflected in a contemporary gradient of intrapopulation variability, which exhibits a correlation with the likely directions of ancient dispersal flows [47]. According to the available data on mtDNA and microsatellite loci variability in sockeye salmon in the Russian Far East, the following picture emerges: the colonization of the West coast of Kamchatka most likely proceeded sequentially from south to north [61,62], while the colonization of the East Coast followed a more complex scenario. Both types of data suggest that the dispersion of sockeye salmon populations along the West Pacific coast originated from multiple refugees.…”

Evolutionary and Ecological Aspects of the Population Structure Formation of Sockeye Salmon Oncorhynchus nerka (Salmonidae) in Western Kamchatka

“…The majority of Asian sockeye salmon populations are widely considered as relatively young by historical standards, and their age does not exceed 10-12 thousand years (Cheshnev, 1998;Brykov et al, 2005), since its modern distribution range largely coincides with the supposed area of the last Wisconsin glaciation (maximum ~26.5−19.0 thousand years ago, deglaciation ~ 16.90−12.68 thousand years ago) in the North Pacific Velichko and Faustova, 1989). Previously, based on the results of the variability analysis of the mtDNA control region, we found that the entire Asian part of the sockeye salmon distribution range is a secondary contact zone resulting from the explosive expansion of this species during the Holocene transgression and the colonization of most of the Kamchatka Peninsula by two genetic lines of sockeye salmon with different origin (i.e., originating from different refugia that probably existed in the general area of Beringia and/or on the American or Eurasian continent) (Khrustaleva et al, 2020). According to Varnavskaya (2006), large regional complexes of sockeye salmon correspond to the dispersal centers of the species, and in areas of large population size, there could be the so-called population nuclei: ancestral populations, from which all other populations in the region originate.…”

Genetic Structuring and Conservation of Asian Sockeye Salmon: Identification of Regional Stock Complexes

“…This glaciation would have acted as a barrier preventing anadromous fish from accessing these watersheds. Previously, based on the results of an analysis of variability in the mtDNA control region, we determined that the entire Asian part of the sockeye salmon range represents a zone of secondary contact resulted from the rapid expansion of this species during the Holocene transgression, leading to the colonization of the majority of watersheds on the Kamchatka Peninsula by two distinct genetic lineages of sockeye salmon with differing origins (i.e., fish from different refugia that probably existed in the Beringia region (the territory of modern Alaska) and in the Kamchatka River basin) (Khrustaleva et al, 2020). These findings were confirmed by the results of admixture analysis in DAPC and in STRUCTURE, according to which all populations of these complexes had a "hybrid" origin, i.e.…”

“…However, between 2006 and 2014, we were able to collect samples from several sockeye salmon nursery lakes on the Kuril and Commander Islands. The study of the polymorphism of the mtDNA control region showed that the sockeye salmon from the lakes of Iturup Island was characterized by moderate haplotype and nucleotide diversity, while the genetic diversity of the sockeye salmon from the Northern Kuriles and Bering Island was significantly lower compared to the continental populations (Khrustaleva, 2016;Khrustaleva et al, 2020). Furthermore, unique haplotypes were found within the South Kuril sockeye salmon populations, which 5 are transitional forms between two Asian mtDNA haplogroups.…”