Full mitochondrial genome sequences reveal new insights about post-glacial expansion and regional phylogeographic structure in the Atlantic silverside (Menidia menidia)
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One of the biggest challenges in population genetics of marine species is to uncover subtle phylogeographic patterns masked by large effective population sizes and/or high gene flow. In this paper, we use 189 full mitochondrial genome sequences from the Atlantic silverside (Menidia menidia), obtained during whole nuclear genome re-sequencing, to address this challenge. With this approach, we were able to provide a high-resolution analysis of the demographic history and current genetic structure of the species. We clearly defined a regional genetic structure that is stronger than previously thought. This structure groups the species into three regional subdivisions: (1) south of Cape Cod; (2) Gulf of Maine; and (3) Gulf of St. Lawrence. Among the regional subdivisions, our data reveal that the two northern groups show the greatest divergence despite their adjacency along the latitudinal gradient, while genetic homogeneity within the southern subdivision suggests connectivity throughout its broad geographical distribution. Furthermore, using approximate Bayesian computation (ABC) methods, we inferred that both northern populations are the result of independent colonization events from the south after the Last Glacial Maximum (LGM). Our analyses indicate that at least one of the northern populations has received two waves of colonization, one timed immediately after the LGM and the other timed after the end of the Younger Dryas glacial re-advance. Finally, we found one locus potentially under positive selection in the mitochondrial genome. The results of this study illustrate the power of full mitochondrial genome sequencing in phylogeographic research, and because the Atlantic silverside is known for its clinal phenotypic variation throughout its range, our findings have important implications for the study of local adaptation.
We are most indebted to Stephen Palumbi, who provided funding and valuable insights to this project. We would also like to thank Steve Munch and Hannes Baumann for helping transport samples for this study, Beth Sheets for assistance in the laboratory, Anna Tigano and two anonymous reviewers for their valuable comments on the manuscript, and Vivienne Liu for helping with the figures. The data were generated with support from National Science Foundation Grant OCE-1434325 to Stephen Palumbi.
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Conflict of interest
The authors declare that they have no conflict of interest.
We declare that all applicable international, national, and/or institutional guidelines for sampling, care, and experimental use of organisms for the study have been followed and all necessary approvals have been obtained.
- Avise JC (2000) Phylogeography: the history and formation of species. Harvard Univ Press, Cambridge, MAGoogle Scholar
- Carpenter KE, Munroe T (2015) Menidia menidia. The IUCN Red List of Threatened Species 2015:e.T16441575A16510092. https://doi.org/10.2305/iucn.uk.2015-4.rlts.t16441575a16510092.en
- Conover DO, Murawski S (1982) Offshore winter migration of the Atlantic silverside, Menidia menidia. Fish Bull 80:145–149Google Scholar
- Cordes JF, Graves JE (2003) Investigation of congeneric hybridization in and stock structure of weakfish (Cynoscion regalis) inferred from analyses of nuclear and mitochondrial DNA loci. Fish Bull 101:443–451Google Scholar
- Cornuet J-M, Pudlo P, Veyssier J, Dehne-Garcia A, Gautier M, Leblois R, Marin J-M, Estoup A (2014) DIYABC v2.0: a software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism, DNA sequence and microsatellite data. Bioinformatics 30:1187–1189CrossRefPubMedGoogle Scholar
- Iwasaki W, Fukunaga T, Isagozawa R, Yamada K, Maeda Y, Satoh TP, Sado T, Mabuchi K, Takeshima H, Miya M, Nishida M (2013) MitoFish and MitoAnnotator: a mitochondrial genome database of fish with an accurate and automatic annotation pipeline. Mol Biol Evol 30:2531–2540CrossRefPubMedPubMedCentralGoogle Scholar
- Jacobsen MW, da Fonseca RR, Bernatchez L, Hansen MM (2016) Comparative analysis of complete mitochondrial genomes suggests that relaxed purifying selection is driving high nonsynonymous evolutionary rate of the NADH2 gene in whitefish (Coregonus ssp.). Mol Phylogenet Evol 95:161–170CrossRefPubMedGoogle Scholar
- Kocher TD, Stepien CA (eds) (1997) Molecular systematics of fishes. Academic Press, San Diego, CAGoogle Scholar
- Morin PA, Archer FI, Foote AD, Vilstrup J, Allen EE, Wade P, Durban J, Parsons K, Pitman R, Li L, Bouffard P, Nielsen SCA, Rasmussen M, Willerslev E, Gilbert MTP, Harkins T (2010) Complete mitochondrial genome phylogeographic analysis of killer whales (Orcinus orca) indicates multiple species. Genome Res 20:908–916CrossRefPubMedPubMedCentralGoogle Scholar
- Nielsen R, Slatkin M (2013) An introduction to population genetics: theory and applications. Sinauer, Sunderland, MAGoogle Scholar
- Rambaut A (2016) FigTree. http://tree.bio.ed.ac.uk/software/figtree/. Accessed 15 Nov 2016
- Rasmussen SO, Andersen KK, Svensson AM, Steffensen JP, Vinther BM, Clausen HB, Siggaard-Andersen M-L, Johnsen SJ, Larsen LB, Dahl-Jensen D, Bigler M, Röthlisberger R, Fischer H, Goto-Azuma K, Hansson ME, Ruth U (2006) A new Greenland ice core chronology for the last glacial termination. J Geophys Res Atmos 111:D06102CrossRefGoogle Scholar
- Setiamarga DHE, Miya M, Yamanoue Y, Mabuchi K, Satoh TP, Inoue JG, Nishida M (2008) Interrelationships of Atherinomorpha (medakas, flyingfishes, killifishes, silversides, and their relatives): the first evidence based on whole mitogenome sequences. Mol Phylogenet Evol 49:598–605CrossRefPubMedGoogle Scholar
- Steffensen JP, Andersen KK, Bigler M, Clausen HB, Dahl-Jensen D, Fischer H, Goto-Azuma K, Hansson M, Johnsen SJ, Jouzel J, Masson-Delmotte V, Popp T, Rasmussen SO, Röthlisberger R, Ruth U, Stauffer B, Siggaard-Andersen M-L, Sveinbjörnsdóttir ÁE, Svensson A, White JWC (2008) High-resolution Greenland ice core data show abrupt climate change happens in few years. Science 321:680–684CrossRefPubMedGoogle Scholar
- Wetterstrand KA (2015) DNA sequencing costs: data from the NHGRI genome sequencing program (GSP). www.genome.gov/sequencingcosts. Accessed 29 May 2017
- Willette D, Allendorf F, Barber P, Barshis D, Carpenter K, Crandall E, Cresko W, Fernandez-Silva I, Matz M, Meyer E, Santos M, Seeb L, Seeb J (2014) So, you want to use next-generation sequencing in marine systems? Insight from the Pan-Pacific Advanced Studies Institute. Bull Mar Sci 90:79–122CrossRefGoogle Scholar