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

Abstract

HighlightsMitochondrial monophyly is commonly employed to define evolutionary significant units.Monophyly may be caused by insufficient sampling or a recent common ancestor.Mitogenomic studies are generally based on few samples and prone to sampling issues.Expanded mitogenome sampling negates previous monophyly in fin whales.AbstractThe 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 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 is 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 most recent common ancestor and hence the probability that individuals in a sample are monophyletic.

A Genetic Perspective on Cetacean Evolution

“…research question is often the result of balancing resources (e.g., samples, funding), capabilities (e.g., skills and facilities), and novelty and scientific interest. For instance, Cabrera et al (2019) analyzed the genealogy of North Atlantic, North Pacific, and Southern Hemisphere fin whales; the authors compared a previously published data set with entire mitochondrial genomes but small sample sizes (n = 154) against a data set with a larger sample size (n = 1,676) but only the control region of the mitochondrial genome. In the latter data set, the authors identified a North Atlantic lineage that was not detected in the former data set of longer sequences but fewer individuals and concluded that the tentative monophyly of the North Atlantic fin whales based on mitochondrial genomes was a result of small sample size.…”