Convergent evolution of skim feeding in baleen whales

摘要

The evolutionary relationships of the pygmy right whale Caperea marginata, the smallest and most enigmatic of the living baleen whales (mysticetes), remain contentious. For 150 years, morphological analyses have allied Caperea with right whales based on their similar skim filter feeding strategies and shared cranial features like a tall braincase, highly arched rostrum, and elongate baleen plates (Beddard, 1901; Bisconti, 2012; Gray, 1871; McLeod et al., 1993). By contrast, molecular and some anatomical evidence—e.g., presence of a squamosal cleft, tympanic recess, and four-fingered flipper—suggest a closer relationship with rorquals and gray whales, Eschrichtius robustus (Dornburg et al., 2012; Fordyce & Marx, 2013; Lloyd & Slater, 2021; Marx, 2011; McGowen et al., 2009, 2020; Park et al., 2017; Steeman et al., 2009). Reconciling these divergent interpretations has proved challenging, with nontraditional anatomical character interpretations that are consistent with the molecular data (e.g., Fordyce & Marx, 2013; Gol'din & Steeman, 2015; Marx & Fordyce, 2016) reputedly “gloss[ing] over the substantial issue of convergence posed by the many balaenid features of Caperea” (Berta & Deméré, 2018, p. 73). As a result, many morphological analyses continue to recover—or regard—Caperea and right whales as sister taxa (Bisconti, 2015; Bisconti & Carnevale, 2022; Bisconti et al., 2017, 2021; Boessenecker & Fordyce, 2017; El Adli et al., 2014; Peredo et al., 2018), which in turn has shaped debates around baleen whale phylogeny, the placement of fossils, and the prevalence and role of convergent feeding evolution. Two substantial knowledge gaps have prevented the emergence of a consensus: (1) an extremely limited pygmy right whale fossil record that currently comprises just six specimens worldwide, all of which already resemble Caperea (Marx et al., 2018); and (2) the lack of full genomic data revealing the true level of molecular support for either hypothesis. Recent advances in genomic sequencing have generated a broad comparative data set that includes right whales, gray whales and rorquals (Árnason et al., 2018), but has not yet included Caperea beyond the level of a subset of individual protein-coding genes (McGowen et al., 2020). Here, we present the first genome of a pygmy right whale in the form of high-coverage whole-genome shotgun data. We extracted genomic DNA from kidney tissue obtained from a juvenile female pygmy right whale (South Australian Museum, Adelaide, specimen M27462) that stranded near Port Vincent, South Australia, in September 2017. The carcass was retrieved on the morning of the day after the animal had perished, and was immediately frozen until the postmortem and tissue collection. DNA extraction was performed using a Kingfisher robot (Thermo Fisher Scientific), following the manufacturer's Blood & Tissue Extraction protocol. Around 10 μg of DNA were provided for library preparation. DNA quality was assessed using a TapeStation to ensure suitability for library preparation. Double-stranded libraries were built using the Illumina TruSeq PCR-free library preparation protocol and then sequenced on an Illumina HiSeqX in high output mode with 2 × 150 bp paired-end sequencing chemistry at SciLifeLab (Uppsala University, Sweden). After sequencing, we mapped both our pygmy right whale data and published genomes for two right whales, the gray whale and five rorquals to the ~2.4 gigabase (Gb) sperm whale reference assembly (Physeter macrocephalus, GCF_002837175.2; Table S1). By mapping to the sperm whale genome, we controlled for bias driven by phylogenetic distance between the target organism and the reference (e.g., Brandt et al., 2015): as an outgroup, the sperm whale is equally distant to all our focal species (Árnason et al., 2018). To infer the phylogenetic placement of Caperea we created a genome-wide species tree, allowing us to quantify and overcome gene tree discordance caused by processes such as incomplete lin