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Full-Text PDF (Accepted Author Manuscript) Galatius, A., Olsen, M. T., Steeman, M. E., Racicot, R. A., Bradshaw, C. D., Kyhn, L. A., & Miller, L. A. (2019). Raising your voice: Evolution of narrow-band high-frequency signals in toothed whales (Odontoceti). Biological Journal of the Linnean Society, 126(2), 213-224. https://doi.org/10.1093/biolinnean/bly194 Peer reviewed version License (if available): Other Link to published version (if available): 10.1093/biolinnean/bly194 Link to publication record in Explore Bristol Research PDF-document This is the accepted author manuscript (AAM). The final published version (version of record) is available online via OUP at https://doi.org/10.1093/biolinnean/bly194 . Please refer to any applicable terms of use of the publisher. University of Bristol - Explore Bristol Research General rights This document is made available in accordance with publisher policies. Please cite only the published version using the reference above. Full terms of use are available: http://www.bristol.ac.uk/red/research-policy/pure/user-guides/ebr-terms/ JOURNAL Biological Journal of the Linnean Society TITLE Raising your voice: Evolution of narrow band high frequency signals in toothed whales (Odontoceti) Short title: Evolution of narrow band high frequency signals AUTHORS Anders Galatiusa,1,2, Morten Tange Olsenb,2, Mette Elstrup Steemanc, Rachel A. Racicotd,e,f, Catherine D. Bradshawg,h, Line A. Kyhni, Lee A. Millerj,3 AFFILIATIONS aDepartment of Bioscience, Aarhus University, 4000 Roskilde, Denmark bEvolutionary Genomics, Natural History Museum of Denmark, University of Copenhagen, 2100 Copenhagen O, Denmark cMuseum of Southern Jutland, Section of Natural History, 6510 Gram, Denmark dW. M. Keck Science Department, Claremont McKenna, Pitzer, and Scripps Colleges, Claremont, CA, 91711 eThe Dinosaur Institute, Natural History Museum of Los Angeles County, Los Angeles, CA 90007, USA fDepartment of Earth and Environmental Sciences, Vanderbilt University, Nashville, TN 37240, USA gSchool of Geographical Sciences, University of Bristol, Bristol, BS8 1TH, UK hMet Office Hadley Centre, Exeter, EX1 3PB, UK iDepartment of Biology, University of Southern Denmark, 5230 Odense, Denmark 1Corresponding author 2These authors contributed equally to the work 3Senior author Correspondence: Anders Galatius; [email protected] 1 ABSTRACT Cetaceans use sound for communication, navigation and finding prey. Most extant odontocetes produce broadband (BB) biosonar clicks covering frequency ranges from tens to 150-170 kHz. In contrast, the biosonar clicks of some odontocetes are unique, being narrow in bandwidth with high centroid frequency (NBHF), peak frequencies being at 125-140 kHz and bandwidths of 11-20 kHz. Thirteen species within four families (Phocoenidae, Pontoporiidae, Kogiidae, Delphinidae) are known to produce these signals, implying convergent evolution under strong selective drivers. Several hypotheses have been proposed, including acoustic crypsis to escape killer whale predation, but none have provided comprehensive explanation of the timing of NBHF evolution and the pressures driving sound production to such extremes. Using molecular phylogenetics and cochlea anatomy of extinct and extant taxa, we demonstrate that early NBHF adaptations occurred at least 10 Ma, and possibly up to 18 Ma, indicating that killer whales cannot have been the sole driving force of NBHF, but that now extinct odontocetes may have provided similar pressures. Using palaeoclimate modelling, we further demonstrate that the upper advantageous spectral window for NBHF signals at around 130 kHz has persisted throughout most of the global sea area since the mid-Miocene, covering all known instances of NBHF evolution. KEY WORDS Anatomy, Biosonar, Climate, Hearing, Palaeontology, Phylogeny 2 INTRODUCTION Hearing is critical for cetaceans. They use sound for communication, navigation, finding prey and avoiding predators. The first cetaceans, the pakicetids, that appeared about 54 million years ago (Ma) were already adapted for underwater hearing. Near-modern underwater hearing mechanisms had evolved about 10 Ma later (Nummela, Thewissen, Bajpai, Hussain & Kumar, 2004). Modifications of hearing and sound production resulting in a biosonar system probably arose about 32 Ma in odontocetes (Churchill, Martinez-Caceres, de Muizon, Mnieckowski & Geisler, 2016; Geisler, Colbert & Carew, 2014), allowing the use of sound for locating prey and underwater orientation. Most extant odontocetes produce broadband (BB) biosonar clicks covering a frequency range from a few tens of kHz to about 150-170 kHz. In contrast, the biosonar clicks of some odontocetes have evolved to an extreme, resulting in a narrow band high frequency (NBHF) biosonar with peak frequencies at 125-140 kHz and rms bandwidth of about 11-20 kHz (Kyhn, 2010). Presently, thirteen species within four families (Delphinidae (Kyhn, Tougaard, Jensen, Wahlberg, Stone, Yoshinaga, Beedholm & Madsen, 2009; Kyhn, Jensen, Beedholm, Tougaard, Hansen & Madsen, 2010), Phocoenidae (Kyhn, Tougaard, Beedholm, Jensen, Ashe, Williams & Madsen, 2013; Li, Wang, Wang & Akamatsu, 2005; Miller & Wahlberg, 2013; Villadsgaard, Wahlberg & Tougaard, 2007), Pontoporiidae (Melcon, Failla & Iniguez, 2012) and Kogiidae (Madsen, Carder, Beedholm & Ridgway, 2005)) are known to produce NBHF signals. Consequently, there appears to have been at least four instances of convergent evolution, implying the presence of strong selective drivers for NBHF biosonar. Although several hypotheses have been proposed (Andersen & Amundin, 1976; Au, 1993; Kyhn, 2010; Madsen et al., 2005; Miller & Wahlberg, 2013; Morisaka & Connor, 2007), none have provided a comprehensive explanation of the timing of NBHF evolution and selection pressures driving sound production to such extremes. The transmission properties of a biosonar system are dictated by the size of the sound producing organ and the spectral properties of the transmitted sound (Au, 1993). Thus, the high 3 centre frequency is likely contingent on the small sizes of NBHF species and it is not surprising that they use centre frequencies above 100 kHz to achieve directivity comparable to larger species (Au, 1993; Au, Kastelein, Rippe & Schooneman, 1999; Au, Pawloski, Nachtigall, Blonz & Gisner, 1995; Koblitz, Wahlberg, Stilz, Madsen, Beedholm & Schnitzler, 2012; Kyhn et al., 2013; Kyhn et al., 2009; Kyhn, 2010; Kyhn et al., 2010). It is therefore the narrow bandwidth of just 11-20 kHz in combination with a high centre frequency that make NBHF signals unique (Götz, Antunes & Heinrich, 2010; Kyhn et al., 2009; Kyhn, 2010; Kyhn et al., 2010; Li et al., 2005; Madsen et al., 2005; Villadsgaard et al., 2007). Most studies have argued that the selective pressure driving signals above 100 kHz was killer whale (Orcinus orca Linneaus, 1758) predation (Andersen & Amundin, 1976; Kyhn et al., 2009; Kyhn, 2010; Kyhn et al., 2010; Madsen et al., 2005; Miller & Wahlberg, 2013; Morisaka & Connor, 2007). Killer whales have poorer hearing above 100 kHz (Branstetter, Leger, Acton, Stewart, Houser, Finneran & Jenkins, 2017), allowing extant NBHF species acoustic crypsis (Morisaka & Connor, 2007). However, such predation could only have been a selective pressure for NBHF signals after the appearance of killer whales. The crown groups of several NHBF species (e.g. Phocoenidae and Pontoporiidae) are much older (Steeman, Hebsgaard, Fordyce, Ho, Rabosky, Nielsen, Rahbek, Glenner, Sorensen & Willerslev, 2009), but it is unclear whether NBHF evolved in these groups before or after the appearance of killer whales. A narrow bandwidth is also advantageous for detecting a signal in masking noise (Møhl, 1973). In this regard, mean noise level at Beaufort sea states 3-5 meets thermal noise at about 130 kHz forming a minimum in ambient ocean noise (Madsen et al., 2005; Madsen & Surlykke, 2014; Mellen, 1952; Miller & Wahlberg, 2013; Wenz, 1962), theoretically providing superior echo-to- noise ratio and setting the upper frequency limit for NBHF signals. To date however, there is a lack of palaeoclimatic data on wind speed and sea states, which could support the hypothesis of ambient ocean noise as a driver of NBHF evolution. 4 We aim to unravel the selection pressures leading to NBHF evolution using molecular phylogenomics and cochlear anatomy of extinct and extant taxa to narrow the potential time windows during which NBHF signals evolved. We further consider whether extinct odontocete predators could have exerted selection pressure for acoustic crypsis in the past. Finally, we use palaeoclimate modelling through millennia to assess whether ambient ocean noise could have provided an advantageous spectral window for NBHF signals. MATERIALS AND METHODS Phylogenetic relationships The phylogenetic context of NBHF evolution and updated estimates of divergence times for odontocetes were explored by a phylogenetic analysis based on mitogenome sequence data from 41 odontocetes and one mysticete (Balaena mysticetus Linneaus, 1758). Data were obtained from NCBI’s Genbank and comprised the 13 protein-coding genes of the mitochondrial genome. Inter- gene regions and the d-loop were omitted due to missing data and to minimize mutation saturation, repetitive sequences and/or alignment ambiguities. Further, the ND6 gene was reverse- complemented, overlapping regions in the ND5, ND6, ATP6, COX3, ATP8 and ATP6 genes were duplicated, and all indels were removed to obtain an 11,388 base pair (bp) sequence with the 13 genes adjusted to the same reading frame. 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