Although humpback whales are among the best-studied of the large whales, population boundaries in the Southern Hemisphere (SH) have remained largely untested. We assess population structure of SH humpback whales using 1,527 samples collected from whales at fourteen sampling sites within the Southwestern and Southeastern Atlantic, the Southwestern Indian Ocean, and Northern Indian Ocean (Breeding Stocks A, B, C and X, respectively). Evaluation of mtDNA population structure and migration rates was carried out under different statistical frameworks. Using all genetic evidence, the results suggest significant degrees of population structure between all ocean basins, with the Southwestern and Northern Indian Ocean most differentiated from each other. Effective migration rates were highest between the Southeastern Atlantic and the Southwestern Indian Ocean, followed by rates within the Southeastern Atlantic, and the lowest between the Southwestern and Northern Indian Ocean. At finer scales, very low gene flow was detected between the two neighbouring sub-regions in the Southeastern Atlantic, compared to high gene flow for whales within the Southwestern Indian Ocean. Our genetic results support the current management designations proposed by the International Whaling Commission of Breeding Stocks A, B, C, and X as four strongly structured populations. The population structure patterns found in this study are likely to have been influenced by a combination of long-term maternally directed fidelity of migratory destinations, along with other ecological and oceanographic features in the region.
Taxonomy is an imprecise science that delimits the evolutionary continuum into discrete categories. For marine mammals, this science is complicated by the relative lack of morphological data for taxa that inhabit remote and often vast ranges. We provide guidelines to promote consistency in studies relying primarily on molecular genetic data to delimit cetacean subspecies from both populations and species. These guidelines identify informational needs: basis for the taxonomic hypothesis being tested, description of current taxonomy, description of relevant life history, sample distribution, sample size, number and sequence length of genetic markers, description of measures taken to ensure data quality, summary statistics for the genetic markers, and analytical methods used to evaluate the genetic data. We propose an initial set of quantitative and qualitative standards based on the types of data and analytical methods most readily available at present. These standards are not expected to be rigidly applied. Rather, they are meant to encourage taxonomic arguments that are consistent and transparent. We hope professional societies, such as the Society for Marine Mammalogy, will adopt quantitative standards that evolve as new data types and analytical methods become widely available.
There are three described subspecies of fin whales (Balaenoptera physalus): B. p. physalus Linnaeus, 1758 in the Northern Hemisphere, B. p. quoyi Fischer, 1829 in the Southern Hemisphere, and a recently described pygmy form, B. p. patachonica Burmeister, 1865. The discrete distribution in the North Pacific and North Atlantic raises the question of whether a single Northern Hemisphere subspecies is valid. We assess phylogenetic patterns using ∼16 K base pairs of the complete mitogenome for 154 fin whales from the North Pacific, North Atlantic - including the Mediterranean Sea - and Southern Hemisphere. A Bayesian tree of the resulting 136 haplotypes revealed several well-supported clades representing each ocean basin, with no haplotypes shared among ocean basins. The North Atlantic haplotypes (n = 12) form a sister clade to those from the Southern Hemisphere (n = 42). The estimated time to most recent common ancestor (TMRCA) for this Atlantic/Southern Hemisphere clade and 81 of the 97 samples from the North Pacific was approximately 2 Ma. 14 of the remaining North Pacific samples formed a well-supported clade within the Southern Hemisphere. The TMRCA for this node suggests that at least one female from the Southern Hemisphere immigrated to the North Pacific approximately 0.37 Ma. These results provide strong evidence that North Pacific and North Atlantic fin whales should not be considered the same subspecies, and suggest the need for revision of the global taxonomy of the species.
Next-generation sequencing (NGS) is emerging as an efficient and cost-effective tool in population genomic analyses of nonmodel organisms, allowing simultaneous resequencing of many regions of multi-genomic DNA from multiplexed samples. Here, we detail our synthesis of protocols for targeted resequencing of mitochondrial and nuclear loci by generating indexed genomic libraries for multiplexing up to 100 individuals in a single sequencing pool, and then enriching the pooled library using custom DNA capture arrays. Our use of DNA sequence from one species to capture and enrich the sequencing libraries of another species (i.e. cross-species DNA capture) indicates that efficient enrichment occurs when sequences are up to about 12% divergent, allowing us to take advantage of genomic information in one species to sequence orthologous regions in related species. In addition to a complete mitochondrial genome on each array, we have included between 43 and 118 nuclear loci for low-coverage sequencing of between 18 kb and 87 kb of DNA sequence per individual for single nucleotide polymorphisms discovery from 50 to 100 individuals in a single sequencing lane. Using this method, we have generated a total of over 500 whole mitochondrial genomes from seven cetacean species and green sea turtles. The greater variation detected in mitogenomes relative to short mtDNA sequences is helping to resolve genetic structure ranging from geographic to species-level differences. These NGS and analysis techniques have allowed for simultaneous population genomic studies of mtDNA and nDNA with greater genomic coverage and phylogeographic resolution than has previously been possible in marine mammals and turtles.
Cetacean taxonomy continues to be in flux and molecular genetic analyses examining alpha taxonomy in cetaceans have relied heavily on the mitochondrial DNA control region. However, there has been little consistency across studies; a variety of metrics and levels of divergence have been invoked when delimiting new cetacean species and subspecies. Using control region sequences, we explored, across pairs of well‐recognized cetacean populations, subspecies, and species, a suite of metrics measuring molecular genetic differentiation to examine which metrics best categorize these taxonomic units. Nei's estimate of net divergence (dA) and percent diagnosability performed best. All but a single, recently diverged species were unambiguously identified using these metrics. Many subspecies were found at intermediate values as expected, allowing separation from both populations and species, but several had levels of divergence equivalent to populations, resulting in underclassification errors using this single marker. Coupling dA with additional measures, such as percent diagnosability, examining appropriate nuclear genetic markers, and interpreting results in a broader biological context will improve taxonomic investigations in cetaceans.
The creation and use of a globally available database of DNA sequences from a standardized gene region has been proposed as a tool for species identification, assessing genetic diversity and monitoring the legal and illegal trade in wildlife species. Here, we contribute to the Barcode of Life Data System and test whether a short region of the mitochondrial cytochrome c oxidase subunit 1 (COX1) gene would reliably distinguish among a suite of commonly hunted African and South American mammal and reptile species. We used universal primers to generate reference barcode sequences of 645 bp for 23 species from five vertebrate families (Crocodilidae, Alligatoridae, Bovidae, Suidae and Cercopithecidae). Primer cocktails yielded high quality barcode sequences for 179 out of 204 samples (87.7%) from all species included in the study. For most taxa, we sequenced multiple individuals to estimate intraspecific sequence variability and document fixed diagnostic characters for species identification. Polymorphism in the COX1 fragment was generally low (mean = 0.24%), while differences between congeneric species averaged 9.77%. Both fixed character differences and tree-based maximum likelihood distance methods unambiguously identified unknown and misidentified samples with a high degree of certainty. Barcode sequences also differentiated among newly identified lineages of African crocodiles and identified unusually high levels of genetic diversity in one species of African duiker. DNA barcoding offers promise as an effective tool for monitoring poaching and commercial trade in endangered species, especially when investigating semi-processed or morphologically indistinguishable wildlife products. We discuss additional benefits of barcoding to ecology and conservation. Keywords Barcode of life Á Caiman Á Crocodiles Á Cytochrome c oxidase subunit 1 (COX1) Á Hunting Á Molecular forensics Á Primates Á Wildlife monitoring Á Maximum likelihood phylogeny Á Ungulates Electronic supplementary material The online version of this article (
Humpback whales (Megaptera novaeangliae) annually undertake the longest migrations between seasonal feeding and breeding grounds of any mammal. Despite this dispersal potential, discontinuous seasonal distributions and migratory patterns suggest that humpbacks form discrete regional populations within each ocean. To better understand the worldwide population history of humpbacks, and the interplay of this species with the oceanic environment through geological time, we assembled mitochondrial DNA control region sequences representing approximately 2700 individuals (465 bp, 219 haplotypes) and eight nuclear intronic sequences representing approximately 70 individuals (3700 bp, 140 alleles) from the North Pacific, North Atlantic and Southern Hemisphere. Bayesian divergence time reconstructions date the origin of humpback mtDNA lineages to the Pleistocene (880 ka, 95% posterior intervals 550-1320 ka) and estimate radiation of current Northern Hemisphere lineages between 50 and 200 ka, indicating colonization of the northern oceans prior to the Last Glacial Maximum. Coalescent analyses reveal restricted gene flow between ocean basins, with long-term migration rates (individual migrants per generation) of less than 3.3 for mtDNA and less than 2 for nuclear genomic DNA. Genetic evidence suggests that humpbacks in the North Pacific, North Atlantic and Southern Hemisphere are on independent evolutionary trajectories, supporting taxonomic revision of M. novaeangliae to three subspecies.
Uncertainty in marine mammal taxonomy is increasingly being addressed using molecular genetic data. We examined 32 peer‐reviewed articles published between 1994 and 2011to review methodological practices, consistency of markers and analytical methods, and overall quality of arguments used when genetic data have been employed to delimit new species and subspecies of marine mammals. The mitochondrial DNA (mtDNA) control region was the primary genetic marker used in these studies, but analytical methods varied greatly across studies. Diagnosability, a common metric for delimiting subspecies with morphological data, was only used through citing of fixed differences in mtDNA sequences. Assignment tests based on microsatellite data were less common but were applied at both taxonomic levels. Nuclear DNA sequence data were rarely used. Basic background material needed to evaluate the strength of arguments, such as distribution and sampling maps, were often missing. For most studies, sample sizes were good, but adequate geographic sampling for broadly distributed taxa was often lacking, diminishing the strength of evidence for taxonomic distinctness. Examining these empirical cases revealed a mixture of sound and inadequate practices for genetic studies of cetacean taxonomy and suggested that improvements could be made to the field by developing standard guidelines.
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