Howl variation across Himalayan, North African, Indian, and Holarctic wolf clades: tracing divergence in the world’s oldest wolf lineages using acoustics

Current Zoology, 2017, 63(3), 341–348 doi: 10.1093/cz/zox001 Advance Access Publication Date: 17 February 2017 Article Article Howl variation across Himalayan, North African, Indian, and Holarctic wolf clades: tracing divergence in the world’s oldest wolf lineages using acoustics Lauren HENNELLYa,*, Bilal HABIBa,*, Holly ROOT-GUTTERIDGEb, Vicente PALACIOSc, and Daniela PASSILONGOd a Department of Animal Ecology and Conservation Biology, Wildlife Institute of India, Dehradun, India,bDepartment of Biology, Syracuse University, New York, 13210, USA, cCavanilles Institute for Biodiversity and Evolutionary Biology, University of Valencia, Avenue de Blasco Iba~nez, Valéncia 46010, Spain, and dRicerca sulla Selvaggina e sui Miglioramenti Ambientali a Fini Faunistici (C.I.R.Se.M.A.F.), Piazzale delle Cascine 18, Firenze, 1-50144, Italy *Address correspondence to Lauren Hennelly, E-mail: ; and Bilal Habib, E-mail: . Received on 26 June 2016; accepted on 1 December 2016 Abstract Vocal divergence within species often corresponds to morphological, environmental, and genetic differences between populations. Wolf howls are long-range signals that encode individual, group, and subspecies differences, yet the factors that may drive this variation are poorly understood. Furthermore, the taxonomic division within the Canis genus remains contended and additional data are required to clarify the position of the Himalayan, North African, and Indian wolves within Canis lupus. We recorded 451 howls from the 3 most basal wolf lineages—Himalayan C. lupus chanco—Himalayan haplotype, North African C. lupus lupaster, and Indian C. lupus pallipes wolves—and present a howl acoustic description within each clade. With an additional 619 howls from 7 Holarctic subspecies, we used a random forest classifier and principal component analysis on 9 acoustic parameters to assess whether Himalayan, North African, and Indian wolf howls exhibit acoustic differences compared to each other and Holarctic wolf howls. Generally, both the North African and Indian wolf howls exhibited high mean fundamental frequency (F0) and short duration compared to the Holarctic clade. In contrast, the Himalayan wolf howls typically had lower mean F0, unmodulated frequencies, and short howls compared to Holarctic wolf howls. The Himalayan and North African wolves had the most acoustically distinct howls and differed significantly from each other and to the Holarctic wolves. Along with the influence of body size and environmental differences, these results suggest that genetic divergence and/or geographic distance may play an important role in understanding howl variation across subspecies. Key words: acoustic variation, Canis lupus, geographic variation, mammal communication. Variation in vocal communication is influenced by many factors, often leading to acoustic divergence across populations and species (Wilkins et al. 2013). Multiple drivers such as environmental conditions (Morton 1975; Slabbekoorn and Smith 2002; Slabbekoorn and Peet 2003; Russo et al. 2007), body size (Badyaev and Leaf C The Author (2017). Published by Oxford University Press. V 1997; Fitch 1997), population differences in mate preferences (Gerhardt 1991), and stochastic forces (Percy et al. 2006; Irwin et al. 2008) have been shown to shape patterns in acoustic variation across a wide range of taxa and further clarify the processes governing acoustic divergence. Understanding these acoustic differences 341 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact Downloaded https://academic.oup.com/cz/article-abstract/63/3/341/3002317 by guest on 02 June 2018 342 contributes to a comprehensive view of the genetic, behavioral, and ecological attributes of a taxon, and often aids in the taxonomic recognition of cryptic species (Narins 1983; Henry 1994; Kingston et al. 2001). Population-level variation in vocalizations is found across a wide range of mammalian species (seals—Terhune 1994; Risch et al. 2007; whales—Ford 1991; Rossi-Santos and Podos 2006; rodents— Conner 1982; Roux et al. 2002; Campbell et al. 2010; primates— Delgado 2007; bats—O’Farrell et al. 2000; Law et al. 2002), yet remains relatively unexplored for most mammal groups compared to other taxa, such as birds. Additional variation in vocalizations of some taxa have been demonstrated at the subspecies, group, and individual levels, including the howl acoustic structure of wolves Canis lupus (individual—Theberge and Falls 1967; Tooze et al. 1990; Palacios et al. 2007; Root-Gutteridge et al. 2014a, 2014b; group—Zaccaroni et al. 2012; subspecies—Kershenbaum et al. 2016). The howl is the main long-distance vocalization and is used for social spacing, reassembly between dispersed individuals, and territorial defense (Harrington and Mech 1979; Nowak et al. 2007). Previous studies have suggested geographic distance may play a role in howl differences across groups, such that distance among wolf packs increases the differences in howl acoustic qualities, producing a regional accent (Zaccaroni et al. 2012; Root-Gutteridge et al. 2014b). On a subspecies level, smaller canid species show a greater diversity of howl-type usages that may reflect differences in vocal production in different sized species, distinct acoustic properties of habitats, or varying emphases on the social role of howling (Kershenbaum et al. 2016). Taken together, this variation in wolf howl acoustic structure may reflect the evolutionary history, morphology, and/or ecology of a population or subspecies. Based on mitochondrial DNA, the wolves of Asia and North Africa appear to have a dynamic and poorly understood phylogeographic history. Recent research has recognized 3 basal lineages of gray wolves: the Himalayan wolf C. lupus chanco—Himalayan haplotype, Indian wolf C. lupus pallipes, and the North African wolf C. lupus lupaster) (Aggarwal et al. 2003; Sharma et al. 2004; Rueness et al. 2011; Gaubert et al. 2012). The Himalayan wolf is the world’s oldest wolf lineage, having diverged from the rest of the wolf clade around 630,000–800,000 years ago. The same studies showed the Indian wolf mitochondrial lineage to be 270,000–400,000 years divergent from the Himalayan lineage and other wolves (Figure 1; Aggarwal et al. 2003; Sharma et al. 2004). Despite the Himalayan and Indian wolf’s unique ancestry, little is known about their ecology, distribution, and behavior—consequently giving little clarity regarding their taxonomic status (Shrotriya et al. 2012). Morphologically, the Himalayan and Indian wolf show no striking differences to other wolf lineages, as Indian and Himalayan wolves Figure 1. Phylogenetic tree displaying the major relationships within (...truncated)