Big and Slow: Phylogenetic Estimates of Molecular Evolution in Baleen Whales (Suborder Mysticeti)

Abstract

Baleen whales are the largest animals that have ever lived. To develop an improved estimation of substitution rate for nuclear and mitochondrial DNA for this taxon, we implemented a relaxed-clock phylogenetic approach using three fossil calibration dates: the divergence between odontocetes and mysticetes approximately 34 million years ago (Ma), between the balaenids and balaenopterids approximately 28 Ma, and the time to most recent common ancestor within the Balaenopteridae approximately 12 Ma. We examined seven mitochondrial genomes, a large number of mitochondrial control region sequences (219 haplotypes for 465 bp) and nine nuclear introns representing five species of whales, within which multiple species-specific alleles were sequenced to account for within-species diversity (1-15 for each locus). The total data set represents >1.65 Mbp of mitogenome and nuclear genomic sequence. The estimated substitution rate for the humpback whale control region (3.9%/million years, My) was higher than previous estimates for baleen whales but slow relative to other mammal species with similar generation times (e.g., human-chimp mean rate > 20%/My). The mitogenomic third codon position rate was also slow relative to other mammals (mean estimate 1%/My compared with a mammalian average of 9.8%/My for the cytochrome b gene). The mean nuclear genomic substitution rate (0.05%/My) was substantially slower than average synonymous estimates for other mammals (0.21-0.37%/My across a range of studies). The nuclear and mitogenome rate estimates for baleen whales were thus roughly consistent with an 8- to 10-fold slowing due to a combination of large body size and long generation times. Surprisingly, despite the large data set of nuclear intron sequences, there was only weak and conflicting support for alternate hypotheses about the phylogeny of balaenopterid whales, suggesting that interspecies introgressions or a rapid radiation has obscured species relationships in the nuclear genome.

Global diversity and oceanic divergence of humpback whales (Megaptera novaeangliae)

“…Sequences spanning 465 bp of the mtDNA control region were compiled from North Pacific [5,25] (n ¼ 396), South Pacific and southeastern Indian Ocean [13] (n ¼ 804), southwestern Atlantic [26] (n ¼ 48), southwestern Indian Ocean [27] (n ¼ 1137) and western North Atlantic [25,28] (n ¼ 348) studies. Blue (Balaenoptera musculus) and fin (Balaenoptera physalus) whales were used as outgroups in phylogenetic reconstructions (GenBank AY582748, NC_001321, NC_001601 and AY582748) following Sasaki et al [29].…”

“…Bayes factors (BFs) were calculated in TRACER to determine the best-fitting population model. We imposed a strict clock with a rate of 3.94% bp 21 Myr 21 for the humpback control region as determined by phylogenetic approaches [25]. To assess the impact of assumed substitution rate, we repeated the analysis using a higher rate of substitution (mean 14 (e) Nuclear diversity, structuring and gene flow Nuclear heterozygosity was estimated for phased alleles and sequences ( p), and F ST and f ST estimates of differentiation between oceans and ocean basins were measured with 50 000 permutations in ARLEQUIN.…”

“…A more representative collection of mitogenomic sequences (e.g. [25]) and additional estimates of populationlevel humpback mutation rates are required to resolve this uncertainty. Sea surface temperatures and ice sheet reconstructions of the Last Glacial Maximum (LGM) suggest that in the North Atlantic the Norwegian Sea was reliably free of ice during the summer months [65], whereas the Gulf of Maine and Scotia Shelf regions show evidence of grounded ice reaching to the continental shelf edge during that period (ca 21 -22 000 years ago) [59].…”

Bucking the trend: genetic analysis reveals high diversity, large population size and low differentiation in a deep ocean cetacean

“…In contrast, high genetic diversity is consistent with long-term stability in population size, whereas low levels of population differentiation suggest connectivity or recent population expansion. As a rule, cetaceans are known to have low genetic diversity in comparison with terrestrial mammals and this is hypothesized to be due to slow mutation rates (Jackson et al, 2009) and demographic factors such as recent population expansion following bottlenecks or behaviour (Oremus et al, 2009).…”

First record of Antarctic minke whale, Balaenoptera bonaerensis, in the northern Gulf of Mexico

“…4). For CAT, the unknown baleen whale sequence was identical to seven GenBank entries for known B. bonaerensis samples from Jackson et al (Jackson et al 2009) and no fixed differences or indels were present in comparison to the other available Antarctic minke whale sequences (Fig. 4).…”