Phylogeography of Asian sockeye salmon (Oncorhynchus nerka) based on the analysis of mtDNA D-loop polymorphism
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1
All-Russian Research Institute Fisheries and Oceanography, Russia
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2
Department of Biology, Lomonosov Moscow State University, Russia
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3
Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, Russia
Sockeye salmon is highly commercially important species in the Far East of Russia. It is widely distributed both on Asian and North American coasts of the Pacific Ocean. It belongs to anadromous salmonids, characterized by strong phylopatry, monocyclicity, and extremely complex hierarchic population structure. It is crucial for sockeye salmon population genetics to understand the main patterns of intraspecies structure formation and evolution. Among widely used genetic markers mtDNA is still the marker of choice for estimation of population diversity and genetic divergence, as well as for study of the pathways of species expansion and reconstruction of the sequence of colonization of new areas in the postglacial periods. The subject of the work was an analysis of the contemporary phylogeography of the species and consideration of possible scenarios for sockeye salmon microevolution in the Asian part of the range using the mtDNA control region (D-loop) sequencing.
In total, 130 specimens of sockeye salmon from different rivers of the mainland part of the range and the Kuril Islands were analyzed (Fig. 1). Primers HN20 and Tpro2 (Brunner et al., 2001) were used for amplification of mtDNA fragments. The sequencing method and statistical approaches are described in detail in (Ponomareva et al., 2018).
After multiple alignments of the sequences 1025 bp region of mtDNA comprising the entire D-loop sequence was examined. 15 polymorphic sites were identified (Table 1). Among the substitutions there were eight transitions, two transversions and five indels (insertion/deletion sites). Most of substitutions were detected in the first and the last quarters of the D-loop sequence, as well as one insertion was registered in the poly-T region.
Two mass haplotypes (hap_1 and hap_2) were revealed; they presented in most samples and differed by 3 substitutions and 2 indels (Table 1). The remaining haplotypes were marked as rare or unique. The genealogy of Asian sockeye salmon D-loop haplotypes was presented in the form of MST-tree excluding indels (Fig. 2). All the sequence variants were distributed among two haplogroups (phylogenetic groups): in the first one hap_1 was the central haplotype, in the second one − hap_2. The star-shaped topology of the tree points to a rapid increase in the diversity of groups, indicating a rapid expansion of the species after reducing its number in the past. Note that the diversity of the second haplogroup is higher, but its main fraction falls on the samples from the middle course of Kamchatka River.
In the geographic distribution of the mass haplotypes frequencies, some patterns can be specified (Fig. 1). Along the coast of the Sea of Okhotsk, the frequencies of mass haplotypes were distributed more or less even. Along the northeastern Kamchatka and Chukotka, the frequencies of both haplotypes were distributed rather mosaically. It can be interpreted as the existence of several species distribution centers during the Late Pleistocene transgressions in this part of the range. In Kamchatka River drainage hap_2 dominated, here also there was observed its greatest diversity. In addition, in the samples from tributaries of the middle course of the river and from Azabach’ye Lake endemic for this basin hap_8 (a variant of hap_1) was revealed. Our data allow us to consider a hypothetical scenario of the formation of the modern sockeye salmon D-loop variability, according to which hap_2 was formed or preserved during the period of the Würm (or Wisconsin) glaciation in a vast paleobasin, a deep-water lake in the Kamakovskaya depression, that existed at that time in the middle course of the Kamchatka River, and was uncovered by ice in the late Pleistocene (Bugaev, Kirichenko, 2008). In addition, refugiums in Asia could located in the basin of Anadyr River, as well as in some parts of the northern coast of the Sea of Okhotsk (Chereshnev, 1998). More southern areas: Sakhalin, Primorye and Hokkaido, were practically not exposed to glaciers (Chereshnev, 1998). We assume that the colonization of the Kuril Islands came from Hokkaido by the carriers of hap_1 haplotype, which, in our opinion, is more ancient and preserved in the southern regions from the first wave of settlement of this species in Asia in the middle Pleistocene.
Genetic peculiarity of Sopochnoye Lake population is most likely a consequence of gene drift under conditions of geographical isolation. Besides the anadromous sockeye a population of predatory kokanee inhabits the lake, and haplotypes hap_6 and hap_7 revealed in the sockeye salmon of this drainage are transitional variants between the haplogroups. The transitional haplotype hap_5 was also found in kokanee from Kronotskoye Like. This population has been isolated for more than ten thousand years as a result of blocking of the valley of Kronotskaya River by volcano Krasheninnikov eruption products (Bugaev, Kirichenko, 2008). Apparently, the ancestral haplotypes could persist in relict sockeye populations (from Southern Kuriles, Kamchatka River, Kronotskoye Like, Anadyr River, and highly likely Pakhacha River), which are characterized by relatively high haplotypic diversity. During the periods of glacial regressions, the ice came from the ocean, so the exit to the sea for anadromous form was closed, and sockeye salmon could persist in the adjacent glacial lakes, reducing in number and turning to a freshwater lifestyle (kokanee).
Fig. 1. Schematic map of sampling locations in Asian Pacific coast (a) and in Kamchatka River drainage (b), and haplotypes frequencies in the samples. Anad – Anadyr River; Ch –Vaamochka Lake; KPh – Pakhacha River; KK − Kamchatka River (outfall); KKrL – Kronotskoye Lake (kokanee); Okh − Okhota River; KP − Palana River; KV − Vorovskaya River; KO − Ozernaya River; NKS − Shumshu Island, Bettobu Lake; NKP − Paramushir Island, Glukhoye Lake; SKIk − Iturup Island, Krasivoye Lake; SKIs − Iturup Island, Sopochnoye Lake; KKa_l − Azabachye Lake (late run); KKhap − Hapiza River; KKel – Elovka River; KKdv − Dvu'yurta River; KKzhup – Zhupanka River.
Fig. 2. Genealogical network of sockeye salmon D-loop haplotypes, built on the base of the minimum number of nucleotide substitutions. The size of the circles and the area of the sectors are proportional to the haplotypes frequency in the corresponding samples.
Table 1. Nucleotide sequences of the Asian sockeye salmon mtDNA D-loop.
References
Brunner, P.C., Douglas, M.R., Osinov, A.G., Wilson, C.C., Bernatchez, L. (2001). Holarctic phylogeography of arctic charr (Salvelinus alpinus L.) inferred from mitochondrial DNA sequences. Evol., 55(3), 573–586.
Bugaev, V.F., Kirichenko, V.E. (2008). Spawning and nursery lakes of Asian sockeye salmon. Petropavlovsk-Kamchatsky: Kamchatpress. 280 p.
Chereshnev, I.A. (1998). Biogeography of freshwater fishes of the Far East in Russia. Vladivostok: Dal’nauka, 131 p.
Ponomareva, E.V., Khrustaleva, А.M., Ponomareva, M.V., Volkov, A.A., Shubina, E.A. (2018). Features of D-loop mtDNA haplotypes diversity of sockeye salmon Oncorhynchus nerka Walbaum. Genetics and breeding of animals. № 2, 45–50.
Keywords:
Sockeye salmon,
Oncorhynchus nerka,
mtDNA,
D-loop,
Phylogeography,
haplotypes geographic distribution
Conference:
XVI European Congress of Ichthyology, Lausanne, Switzerland, 2 Sep - 6 Sep, 2019.
Presentation Type:
Oral
Topic:
TAXONOMY, PHYLOGENY AND ZOOGEOGRAPHY
Citation:
Khrustaleva
A,
Ponomareva
M,
Shubina
E and
Ponomareva
E
(2019). Phylogeography of Asian sockeye salmon (Oncorhynchus nerka) based on the analysis of mtDNA D-loop polymorphism.
Front. Mar. Sci.
Conference Abstract:
XVI European Congress of Ichthyology.
doi: 10.3389/conf.fmars.2019.07.00123
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Received:
22 Jul 2019;
Published Online:
14 Aug 2019.
*
Correspondence:
Mrs. Anastasia Khrustaleva, All-Russian Research Institute Fisheries and Oceanography, Moscow, Moscow Oblast, Russia, mailfed@mail.ru
Mrs. Ekaterina Ponomareva, Department of Biology, Lomonosov Moscow State University, Moscow, Moscow Oblast, 119991, Russia, kponom@mail.ru