Fin whale (Balaenoptera physalus) mitogenomics: A cautionary tale of defining sub-species from mitochondrial sequence monophyly

© The Authors, 2019. This article is distributed under the terms of the Creative Commons Attribution-Noncommercial-Share Alike 4.0 International License. The definitive version was published in Molecular Phylogenetics and Evolution (2019), doi:10.1016/j.ympev.2019.02.003.The advent of massive parallel sequencing technologies has resulted in an increase of studies based upon complete mitochondrial genome DNA sequences that revisit the taxonomic status within and among species. Spatially distinct monophyly in such mitogenomic genealogies, i.e., the sharing of a recent common ancestor among con-specific samples collected in the same region has been viewed as evidence for subspecies. Several recent studies in cetaceans have employed this criterion to suggest subsequent intraspecific taxonomic revisions. We reason that employing intra-specific, spatially distinct monophyly at non-recombining, clonally inherited genomes is an unsatisfactory criterion for defining subspecies based upon theoretical (genetic drift) and practical (sampling effort) arguments. This point was illustrated by a re-analysis of a global mitogenomic assessment of fin whales, Balaenoptera physalus spp., published by Archer et al. (2013), which proposed to further subdivide the Northern Hemisphere fin whale subspecies, B. p. physalus. The proposed revision was based upon the detection of spatially distinct monophyly among North Atlantic and North Pacific fin whales in a genealogy based upon complete mitochondrial genome DNA sequences. The extended analysis conducted in this study (1,676 mitochondrial control region, 162 complete mitochondrial genome DNA sequences and 20 microsatellite loci genotyped in 358 samples) revealed that the apparent monophyly among North Atlantic fin whales reported by Archer et al. (2013) to be due to low sample sizes. In conclusion, defining sub-species from monophyly (i.e., the absence of para- or polyphyly) can lead to erroneous conclusions due to relatively “trivial” aspects, such as sampling. Basic population genetic processes (i.e., genetic drift and migration) also affect the time to the most recent common ancestor and hence the probability that individuals in a sample are monophyletic.We are grateful to Hanne Jørgensen, Anna Sellas, Mary Beth Rew and Christina Færch-Jensen for technical assistance. We thank Drs. P. E. Rosel and K. D. Mullin (U.S. National Marine Fisheries Service Southeast Fisheries Science Center) and members of the U.S. Northeast and Southeast Region Marine Mammal Stranding Network and its response teams, including the International Fund for Animal Welfare, the Marine Mammal Stranding Center, Mystic Aquarium, the Riverhead Foundation for Marine Research and Preservation (K. Durham) and the Marine Mammal Stranding Program of the University of North Carolina Wilmington for access to fin whale samples from the western North Atlantic. We thank Gisli Vikingsson for providing samples. We are indebted to Dr. Eduardo Secchi for facilitating data sharing. Data collection in the Southern Ocean was conducted under research projects Baleias (CNPq grants 557064/2009-0 and 408096/2013-6), INTERBIOTA (CNPq 407889/2013-2) and INCT-APA (CNPq 574018/2008-5), of the Brazilian Antarctic Program and a contribution by the research consortium ‘Ecology and Conservation of Marine Megafauna – EcoMega-CNPq’. MAS was supported through a FCT Investigator contract funded by POPH, QREN European Social Fund, and Portuguese Ministry for Science and Education. Data collection in the Azores was funded by TRACE-PTDC/MAR/74071/2006 and MAPCET-M2.1.2/F/012/2011 [FEDER, COMPETE, QREN European Social Fund, and Proconvergencia Açores/EU Program]. Fin whale illustration herein is used with the permission of Frédérique Lucas. We acknowledge the Center for Information Technology of the University of Groningen for IT support and access to the Peregrine high performance-computing cluster