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Beringian sub-refugia revealed in blackfish (Dallia): implications for understanding the effects of Pleistocene glaciations on Beringian taxa and other Arctic aquatic fauna.
BMC Evol Biol. 2015 Jul 19; 15:144.BE

Abstract

BACKGROUND

Pleistocene climatic instability had profound and diverse effects on the distribution and abundance of Arctic organisms revealed by variation in phylogeographic patterns documented in extant Arctic populations. To better understand the effects of geography and paleoclimate on Beringian freshwater fishes, we examined genetic variability in the genus Dallia (blackfish: Esociformes: Esocidae). The genus Dallia groups between one and three nominal species of small, cold- and hypoxia-tolerant freshwater fishes restricted entirely in distribution to Beringia from the Yukon River basin near Fairbanks, Alaska westward including the Kuskokwim River basin and low-lying areas of Western Alaska to the Amguema River on the north side of the Chukotka Peninsula and Mechigmen Bay on the south side of the Chukotka Peninsula. The genus has a non-continuous distribution divided by the Bering Strait and the Brooks Range. We examined the distribution of genetic variation across this range to determine the number and location of potential sub-refugia within the greater Beringian refugium as well as the roles of the Bering land bridge, Brooks Range, and large rivers within Beringia in shaping the current distribution of populations of Dallia. Our analyses were based on DNA sequence data from two nuclear gene introns (S7 and RAG1) and two mitochondrial genome fragments from nineteen sampling locations. These data were examined under genetic clustering and coalescent frameworks to identify sub-refugia within the greater Beringia refugium and to infer the demographic history of different populations of Dallia.

RESULTS

We identified up to five distinct genetic clusters of Dallia. Four of these genetic clusters are present in Alaska: (1) Arctic Coastal Plain genetic cluster found north of the Brooks Range, (2) interior Alaska genetic cluster placed in upstream locations in the Kuskokwim and Yukon river basins, (3) a genetic cluster found on the Seward Peninsula, and (4) a coastal Alaska genetic cluster encompassing downstream Kuskokwim River and Yukon River basin sample locations and samples from Southwest Alaska not in either of these drainages. The Chukotka samples are assigned to their own genetic cluster (5) similar to the coastal Alaska genetic cluster. The clustering and ordination analyses implemented in Discriminant Analysis of Principal Components (DAPC) and STRUCTURE showed mostly concordant groupings and a high degree of differentiation among groups. The groups of sampling locations identified as genetic clusters correspond to geographic areas divided by likely biogeographic barriers including the Brooks Range and the Bering Strait. Estimates of sequence diversity (θ) are highest in the Yukon River and Kuskokwim River drainages near the Bering Sea. We also infer asymmetric migration rates between genetic clusters. The isolation of Dallia on the Arctic Coastal Plain of Alaska is associated with very low estimated migration rates between the coastal Alaska genetic cluster and the Arctic Coastal Plain genetic cluster.

CONCLUSIONS

Our results support a scenario with multiple aquatic sub-refugia in Beringia during the Pleistocene and the preservation of that structure in extant populations of Dallia. An inferred historical presence of Dallia across the Bering land bridge explains the similarities in the genetic composition of Dallia in West Beringia and western coastal Alaska. In contrast, historic and contemporary isolation across the Brooks Range shaped the distinctiveness of present day Arctic Coastal Plain Dallia. Overall this study uncovered a high degree of genetic structuring among populations of Dallia supporting the idea of multiple Beringian sub-refugia during the Pleistocene and which appears to be maintained to the present due to the strictly freshwater nature and low dispersal ability of this genus.

Authors+Show Affiliations

Department of Biology and Wildlife, University of Alaska Fairbanks, Fairbanks, AK, 99775, USA. m.campbell1@massey.ac.nz. Institute of Fundamental Sciences, Massey University, Palmerston North, 4442, New Zealand. m.campbell1@massey.ac.nz.Department of Biology and Wildlife, University of Alaska Fairbanks, Fairbanks, AK, 99775, USA. ntakebayashi@alaska.edu. Institute of Arctic Biology, University of Alaska Fairbanks, Fairbanks, AK, 99775, USA. ntakebayashi@alaska.edu.School of Fisheries and Ocean Sciences, University of Alaska Fairbanks, Fairbanks, AK, 99775, USA. jalopez2@alaska.edu. University of Alaska Museum, Fairbanks, AK, 99775, USA. jalopez2@alaska.edu.

Pub Type(s)

Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

Language

eng

PubMed ID

26187279

Citation

Campbell, Matthew A., et al. "Beringian Sub-refugia Revealed in Blackfish (Dallia): Implications for Understanding the Effects of Pleistocene Glaciations On Beringian Taxa and Other Arctic Aquatic Fauna." BMC Evolutionary Biology, vol. 15, 2015, p. 144.
Campbell MA, Takebayashi N, López JA. Beringian sub-refugia revealed in blackfish (Dallia): implications for understanding the effects of Pleistocene glaciations on Beringian taxa and other Arctic aquatic fauna. BMC Evol Biol. 2015;15:144.
Campbell, M. A., Takebayashi, N., & López, J. A. (2015). Beringian sub-refugia revealed in blackfish (Dallia): implications for understanding the effects of Pleistocene glaciations on Beringian taxa and other Arctic aquatic fauna. BMC Evolutionary Biology, 15, 144. https://doi.org/10.1186/s12862-015-0413-2
Campbell MA, Takebayashi N, López JA. Beringian Sub-refugia Revealed in Blackfish (Dallia): Implications for Understanding the Effects of Pleistocene Glaciations On Beringian Taxa and Other Arctic Aquatic Fauna. BMC Evol Biol. 2015 Jul 19;15:144. PubMed PMID: 26187279.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Beringian sub-refugia revealed in blackfish (Dallia): implications for understanding the effects of Pleistocene glaciations on Beringian taxa and other Arctic aquatic fauna. AU - Campbell,Matthew A, AU - Takebayashi,Naoki, AU - López,J Andrés, Y1 - 2015/07/19/ PY - 2014/12/03/received PY - 2015/06/08/accepted PY - 2015/7/19/entrez PY - 2015/7/19/pubmed PY - 2015/12/15/medline SP - 144 EP - 144 JF - BMC evolutionary biology JO - BMC Evol. Biol. VL - 15 N2 - BACKGROUND: Pleistocene climatic instability had profound and diverse effects on the distribution and abundance of Arctic organisms revealed by variation in phylogeographic patterns documented in extant Arctic populations. To better understand the effects of geography and paleoclimate on Beringian freshwater fishes, we examined genetic variability in the genus Dallia (blackfish: Esociformes: Esocidae). The genus Dallia groups between one and three nominal species of small, cold- and hypoxia-tolerant freshwater fishes restricted entirely in distribution to Beringia from the Yukon River basin near Fairbanks, Alaska westward including the Kuskokwim River basin and low-lying areas of Western Alaska to the Amguema River on the north side of the Chukotka Peninsula and Mechigmen Bay on the south side of the Chukotka Peninsula. The genus has a non-continuous distribution divided by the Bering Strait and the Brooks Range. We examined the distribution of genetic variation across this range to determine the number and location of potential sub-refugia within the greater Beringian refugium as well as the roles of the Bering land bridge, Brooks Range, and large rivers within Beringia in shaping the current distribution of populations of Dallia. Our analyses were based on DNA sequence data from two nuclear gene introns (S7 and RAG1) and two mitochondrial genome fragments from nineteen sampling locations. These data were examined under genetic clustering and coalescent frameworks to identify sub-refugia within the greater Beringia refugium and to infer the demographic history of different populations of Dallia. RESULTS: We identified up to five distinct genetic clusters of Dallia. Four of these genetic clusters are present in Alaska: (1) Arctic Coastal Plain genetic cluster found north of the Brooks Range, (2) interior Alaska genetic cluster placed in upstream locations in the Kuskokwim and Yukon river basins, (3) a genetic cluster found on the Seward Peninsula, and (4) a coastal Alaska genetic cluster encompassing downstream Kuskokwim River and Yukon River basin sample locations and samples from Southwest Alaska not in either of these drainages. The Chukotka samples are assigned to their own genetic cluster (5) similar to the coastal Alaska genetic cluster. The clustering and ordination analyses implemented in Discriminant Analysis of Principal Components (DAPC) and STRUCTURE showed mostly concordant groupings and a high degree of differentiation among groups. The groups of sampling locations identified as genetic clusters correspond to geographic areas divided by likely biogeographic barriers including the Brooks Range and the Bering Strait. Estimates of sequence diversity (θ) are highest in the Yukon River and Kuskokwim River drainages near the Bering Sea. We also infer asymmetric migration rates between genetic clusters. The isolation of Dallia on the Arctic Coastal Plain of Alaska is associated with very low estimated migration rates between the coastal Alaska genetic cluster and the Arctic Coastal Plain genetic cluster. CONCLUSIONS: Our results support a scenario with multiple aquatic sub-refugia in Beringia during the Pleistocene and the preservation of that structure in extant populations of Dallia. An inferred historical presence of Dallia across the Bering land bridge explains the similarities in the genetic composition of Dallia in West Beringia and western coastal Alaska. In contrast, historic and contemporary isolation across the Brooks Range shaped the distinctiveness of present day Arctic Coastal Plain Dallia. Overall this study uncovered a high degree of genetic structuring among populations of Dallia supporting the idea of multiple Beringian sub-refugia during the Pleistocene and which appears to be maintained to the present due to the strictly freshwater nature and low dispersal ability of this genus. SN - 1471-2148 UR - https://www.unboundmedicine.com/medline/citation/26187279/Beringian_sub_refugia_revealed_in_blackfish__Dallia_:_implications_for_understanding_the_effects_of_Pleistocene_glaciations_on_Beringian_taxa_and_other_Arctic_aquatic_fauna_ L2 - https://bmcevolbiol.biomedcentral.com/articles/10.1186/s12862-015-0413-2 DB - PRIME DP - Unbound Medicine ER -