Masters Et Al 2017

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Zoological Journal of the Linnean Society, 2017, 181, 229–241. With 7 figures.

A new genus for the eastern dwarf galagos (Primates: Galagidae)

JUDITH C. MASTERS1,2*, FABIEN GÉNIN2, SÉBASTIEN COUETTE3,4, COLIN P. GROVES5, STEPHEN D. NASH6, MASSIMILIANO DELPERO7 and LUCA POZZI8,9

1African Primate Initiative for Ecology and Speciation, Department of Zoology & Entomology, University of Fort Hare, Alice 5700, South Africa 2Africa Earth Observatory Network – Earth Systems Science Research Institute, Nelson Mandela Metropolitan University, Port Elizabeth 6031, South Africa 3Biogéosciences, UMR CNRS 6282, Université de Bourgogne Franche-Comté, 6 Boulevard Gabriel, 21000 Dijon, France 4EPHE, PSL Research University, 75014 Paris, France 5School of Archaeology and Anthropology, Australian National University, Canberra, ACT 2601, Australia 6Conservation International, 10 Bayles Avenue, Stony Brook, NY 11790-2122, United States of America. 7Dipartimento di Scienze della Vita e Biologia dei Sistemi - Life Sciences and Systems Biology, Università degli Studi di Torino, Via Accademia Albertina, 13, 10123 Torino, Italy 8Behavioral Ecology and Sociobiology Unit, German Primate Center, Leibniz Institute for Primate Research, 37077 Göttingen, Germany 9Department of Anthropology, The University of Texas at San Antonio, TX 78249, United States of America

Received 29 June 2016; revised 21 October 2016; accepted for publication 19 November 2016

The family Galagidae (African galagos or bushbabies) comprises five genera: Euoticus Gray, 1872; Galago Geoffroy Saint-Hilaire, 1796; Galagoides Smith, 1833; Otolemur Coquerel, 1859; and Sciurocheirus Gray, 1872, none of which is regarded as monotypic, but some (Euoticus and Otolemur) certainly qualify as oligotypic. We argue for the recognition of a sixth genus, if the taxonomy is to reflect galagid evolution accurately. Genetic evidence has consistently demonstrated that the taxa currently referred to the genus Galagoides are not monophyletic but form two clades (a western and an eastern clade) that do not share an exclusive common ancestor; we review 20 years of genetic studies that corroborate this conclusion. Further, we compare vocalizations emitted by small-bodied galagids with proposed phylogenetic relationships and demonstrate congruence between these data sets. Morphological evidence, however, is not entirely congruent with genetic reconstructions; parallel dwarfing in the two clades has led to convergences in skull size and shape that have complicated the classification of the smaller species. We present a craniodental morphometric analysis of small-bodied galagid genera that identifies distinguishing characters for the genera and supports our proposal that five taxa currently subsumed under Galagoides (Galagoides cocos, Galagoides granti, Galagoides orinus, Galagoides rondoensis and Galagoides zanzibaricus) be placed in their own genus, for which we propose the name Paragalago.

ADDITIONAL KEYWORDS: biogeography – bushbaby – craniodental morphometrics – Galagoides – molecular phylogeny – Paragalago –vocalizations.

INTRODUCTION *Corresponding author. E-mail: [email protected] [Version of Record, published online 08 February 2017; http:// In A Field Guide to the Larger Mammals of Africa (Dorst zoobank.org/urn:lsid:zoobank.org:pub:95D93F42-A273-4029- & Dandelot, 1970), Pierre Dandelot illustrated five spe- 8ACB-EAF5D06969F5] cies of galagos (or bushbabies) and two species of pottos.

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Four of the galagid taxa were subsumed under the genus ‘Zanzibar’ galagos (Galagoides cocos, Galagoides granti Galago: that is Galago alleni, Galago crassicaudatus, and Galagoides zanzibaricus) and the squirrel galagos Galago demidovi (sic, now referred to as Galago demi- (Galagoides alleni, s.l.). Honess & Bearder (1996) and doff in accordance with its initial description: Jenkins, Kingdon (1997) recognized three new dwarf galago spe- 1987; Groves, 2001) and Galago senegalensis. The nee- cies just before the turn of the 21st century: Galagoides dle-clawed galagos were classified in their own genus, orinus, originally described by Lawrence and Washburn Euoticus, in accordance with the taxonomies of Schwarz (1936) as a subspecies of Gs. demidoff from the Uluguru (1931), Simpson (1945) and Hill (1953). Forty-five years Mountains, Galagoides rondoensis from the Rondo pla- later, all five taxa are regarded as distinct genera, none teau and Galagoides udzungwensis from the Udzungwa of which is generally viewed as monotypic, although Mountains. All three localities are in Tanzania. Galagoides much of the detailed research has yet to be conducted. In udzungwensis has since been downgraded to a subspe- this contribution, we discuss evidence that Galagoides, cies of Gs. zanzibaricus confined to the Tanzanian main- as construed by Olson (1979) on morphological grounds, land, while Gs. z. zanzibaricus is reserved for the form on does not constitute a clade in molecular phylogenetic Zanzibar Island. Galagoides orinus and Gs. rondoensis reconstructions (DelPero et al., 2000; Masters et al., are now recognized as valid species. 2007; Fabre, Rodrigues & Douzery, 2009; Springer et The morphological characters uniting Olson’s (1979) al., 2012; Pozzi, Disotell & Masters, 2014; Pozzi et al., genus Galagoides were not made explicit, but from our 2015; Pozzi, 2016), and its members are unlikely to have own observations (Groves, 2001; Masters & Couette, shared an exclusive common ancestor. More specifically, 2015) they include moderate basicranial flexion (i.e. the dwarf galagos confined to the forests of East and stronger than in most lemuriforms and lorisids, but not southern Africa require the designation of a new genus. as strong as in the genera Galago or Euoticus), anterior In the subsequent text, we abbreviate Galagoides as Gs. upper premolar (P2) not caniniform (sometimes with a to distinguish it from the abbreviation of Galago (G.). hypocone), third upper molar (M3) ≥ posterior upper premolar (P4) and premaxillaries extended into a tube that projects way beyond the lower jaw. The premaxillary tube HISTORY OF GALAGID GENERA is longest in dwarf galagos, moderate in ‘Zanzibar’ gala- The first galagid genus to enter the scientific literature gos and least pronounced in squirrel galagos. Euoticus, was Galago, described by Etienne Geoffroy Saint-Hilaire Galago and Otolemur have no premaxillary tube and (1796) and was based on a lesser galago specimen col- the anterior margin of the snout is square in shape; in lected in Senegal, West Africa. The name was taken from the absence of a tube, the square-snouted galagos have the Senegalese vernacular name for these animals. The a relictual nub on the midline beneath the nasal aper- genus Galagoides was proposed by Sir Andrew Smith ture, suggesting that extended premaxillaries may have (1833) to distinguish the dwarf (G. demidoff) and lesser been the ancestral condition. Among the lorisids, the (G. senegalensis) galagos from what Smith considered to two small-bodied genera, Arctocebus and Loris, have be the ‘true Galagos’ among which he included species premaxillary tubes. Galagoides is further characterized now referred to the genera Microcebus and Otolemur. by small body size (smaller in the western clade than in Galagoides is now restricted to the dwarf galago taxa. the squirrel galagos or most taxa of the eastern clade), a Otolemur was introduced as the generic epithet to concave nasal profile and dark circumocular rings that denote the greater galagos by Charles Coquerel (1859) range in colour from dark brown to black, separated by a with Otolemur agisymbanus (= garnettii) from Zanzibar grey to white nose stripe. While the deep russet coloura- as the type species. The genus Euoticus, which distin- tion of squirrel galagos makes them instantly recogniz- guishes the needle-clawed species, was introduced ini- able, a survey of other museum specimens designated tially by John Gray (1863) as a subgenus under the as Galagoides revealed variable pelage colouration, both genus Otogale, which also included the greater galagos. within and between populations. In most cases, the ani- A few years later, he elevated Euoticus to the status of mals were covered in dense, soft hairs with dark grey a full genus (Gray, 1872). In the same publication, Gray roots, but brown to bright russet tips on the head, dor- (1872) proposed Sciurocheirus as the generic designa- sum and outer surfaces of the limbs. The tips of the hairs tion of a squirrel galago specimen (Sciurocheirus alleni, on the under surfaces are yellow buff to white, and the s.l.) deriving from Fernando Po (Bioko Island). animals have brown to blackish tails. The genus Galagoides was redefined on morphological grounds by Olson (1979) and employed subsequently OVERVIEW OF MOLECULAR GENETIC by many authors (Honess & Bearder, 1996; Kingdon, EVIDENCE FOR RELATIONSHIPS AMONG 1997; Wickings, Ambrose & Bearder, 1998; DelPero et al., GALAGID LINEAGES 2000; Masters & Bragg, 2000; Masters & Brothers, 2002; Butynski et al., 2006). It comprised the true dwarf gala- Genetic studies – from their earliest days – have consist- gos (Galagoides demidoff and Galagoides thomasi), the ently indicated that Galagoides is polyphyletic, implying

that the grouping based on morphological similarity is (2009) and Fabre et al. (2009). The tree of Masters et al. probably based on plesiomorphic or homoplastic char- (2007) also depicted Galagoides as polyphyletic but did acters. The first such evidence came from allozymes not group Gs. zanzibaricus with the genus Galago. More (Masters et al., 1994), highly repeated DNA sequences recently, a more comprehensive phylogenetic study of (Crovella, Masters & Rumpler, 1994) and 12S ribosomal primates supported a sister taxon relationship between mitochondrial DNA sequences (rDNA; Bayes, 1998). the Zanzibar galagos and the Otolemur/Sciurocheirus All of these studies reconstructed the taxon called Gs. clade, with Gs. demidoff and Gs. thomasi again forming alleni (s.l.) as the sister taxon to Otolemur spp., although an independent clade (Springer et al., 2012). morphological synapomorphies for this group remain The disagreement among these studies regarding elusive. The only shared character Masters & Brothers the phylogenetic placement of the eastern and western (2002) identified from their data set was large, square, lineages may be related to incomplete lineage sorting bunodont molars, indicative of a predominantly frugivo- (or the failure of two or more lineages in a population rous diet and potentially homoplastic. The first Zanzibar to coalesce, leading one of the lineages to coalesce first galago sequences were published by DelPero et al. (2000). with a lineage from a less closely related population) The specimen sampled was probably Gs. granti, as it had or possibly past introgression events, as they were all been collected in northern Mozambique, but was clas- based solely on mitochondrial sequences. To address this sified as Gs. zanzibaricus on the basis of craniodental problem, Pozzi et al. (2014) assembled a molecular data morphometrics (Masters & Bragg, 2000). Using partial set including 27 independent nuclear loci and inferred sequences of three mitochondrial genes (12S and 16S phylogenetic relationships using coalescent-based spe- rDNA and cytochrome b), DelPero and colleagues recon- cies tree methods to account for incomplete lineage sort- structed Gs. demidoff and the so-called Gs. zanzibaricus ing. Their results strongly confirmed the polyphyletic as independent lineages that showed higher levels of status of Galagoides, as well as a sister taxon relation- genetic divergence from one another than either line- ship between the eastern clade and the lesser galagos age showed from any other galagid taxon in their sam- (Galago spp.). The largest molecular data set compiled ple of eight taxa. This result, coupled with the alliance for galagids to date, combining 53 nuclear loci and three of Gs. alleni with Otolemur, led DelPero et al. (2000) to mitochondrial genes, confirmed these results (Pozzi, describe the genus Galagoides as a ‘wastebasket taxon 2016). Figure 1 represents our current understanding of of plesiomorphic species’. This contention has been sup- relationships among the lorisoid primates based on both ported by more recent and more comprehensive stud- nuclear and mitochondrial sequence data, derived from ies. The squirrel galagos continue to be recovered as the the studies of Pozzi et al. (2014, 2015) and Pozzi (2016). sister to the Otolemur clade, and Gray’s (1872) genus, Despite these large nuclear data sets, the sister Sciurocheirus, has been resuscitated (Grubb et al., group relationships of two eastern dwarf galagos, Gs. 2003; Masters et al., 2007). Despite the paucity of mor- rondoensis and Gs. orinus, remain unresolved because phological synapomorphies for this grouping, it derives of limited representative specimens and genetic data; support from the sparse fossil record. Wesselman (1984) a handful of specimens is distributed across museum described a fossil hypodigm from approximately 3-Myr collections in North America and Europe. A molecular sediments in Ethiopia that comprises a fragmentary study based on complete mitochondrial cytochrome b

maxilla, an isolated M2 and an edentulous mandible. On sequences strongly supported an affinity between these the basis of its bunodont teeth and its intermediate size species and the Zanzibar galagos to the exclusion of the between Otolemur and Sciurocheirus, he interpreted the western Galagoides clade (Pozzi et al., 2015), leading taxon (now termed Otolemur howelli; Harrison, 2010) as us to include them in the proposed new genus, which a member of the Sciurocheirus/Otolemur clade, with its hence comprises five species distributed in forests east closest affinities to Otolemur. of the African rift and distinct from the true dwarf gala- Following the removal of the squirrel galagos from gos, Gs. demidoff and Gs. thomasi, in the west (Fig. 2). Galagoides, the western and eastern dwarf galagos have continued to be reconstructed as paraphyletic or even polyphyletic in molecular analyses, indicating that OVERVIEW OF EVIDENCE FROM the genus still includes two independent clades that did VOCAL REPERTOIRES not share an exclusive common ancestor. The western clade comprises the ‘true’ dwarf galagos, Gs. demidoff Vocalizations are particularly important indicators and Gs. thomasi, and the eastern clade includes Gs. of galagid diversity because, as nocturnal animals, zanzibaricus and its allies. Using complete sequences galagos do not rely on morphologically encoded visual of the cytochrome b gene, Roos, Schmitz & Zischler signals for the location and attraction of conspecific (2004) recovered Gs. demidoff as the first galagid line- mates. Many galagid species and species groups have age to diverge and Gs. zanzibaricus as the sister taxon been identified on the basis of differences in loud calls of Galago, a topology supported by Chatterjee et al. (or advertisement calls), which has led to their being

Figure 1. Phylogenetic relationships among galagos. The tree represents a summary of our current understanding of relationships among the lorisoid primates based on both nuclear and mitochondrial sequence data, derived from the studies of Pozzi et al. (2014, 2015) and Pozzi (2016). The western dwarf galago clade is identified by a red rectangle, while the eastern clade is enclosed within a blue square.

grouped according to call structures: crescendo callers, be highly conserved phylogenetically, making them scaling callers, rolling callers, incremental callers and more useful as grouping criteria at deeper phyloge- repetitive callers (Bearder et al., 1996; Kingdon, 1997; netic levels. Vocal homologies among the small-bodied Butynski, Kingdon & Kalina, 2013). Like all char- galagos (i.e. excluding Sciurocheirus and Otolemur acters that are crucial to specific mate recognition, spp.) can be identified in at least three call types: two specific loud calls are qualitatively different between anti-predatory calls (mobbing yaps and buzzy alarms; closely related species, and the rapidity of their evolu- Génin et al., 2016) and the loud socio-territorial calls. tion may obscure their phylogenetic signal at older lev- These vocal homologies are congruent with phyloge- els of divergence (Masters, 2007). For instance, rolling netic relationships among these lineages indicated by and crescendo calls are polyphyletic when compared molecular analyses and further justify the creation of with species relationships determined by molecular a new genus for the eastern dwarf galagos. sequence data, indicating a degree of homoplasy: Gs. granti and Gs. cocos both are described as crescendo callers (Bearder et al., 1996; Kingdon, 1997; Butynski Mobbing yaps et al., 2013), whereas Gs. zanzibaricus, which is recon- The mobbing yap is emitted by all small-bodied gala- structed as the sister taxon to Gs. cocos (see Fig. 1), gos under similar contexts and is often recorded while is a rolling caller, just like Gs. rondoensis. In contrast an animal is circling around to face the observer (FG, to advertisement calls, anti-predatory calls tend to personal observations). It appears to be homologous

Figure 2. Map showing approximate geographic ranges of the two independent dwarf galago clades, Galagoides (red) and the eastern dwarf galagos (blue). The type localities of the species comprising the genera are indicated by symbols. In the case of Galagoides demidoff, the type locality is estimated from Fischer’s (1806) description.

to the loud call of Euoticus spp. (Fig. 3). It is a high- with different contexts, indicating that the various frequency atonal call repeated at frequent intervals, calls evolved different functions associated with dif- often after the emission of a few buzzy alarms. The ferent habitats and socio-territorial systems. On the wide frequency range covered by the call that makes it basis of our own observations as well as those of other sound atonal to human ears is due to very rapid modu- authors (Bearder et al., 1996; Kingdon, 1997; Butynski lation that is likely to be perceived by the animals. et al., 2013), western Galagoides spp. are crescendo callers; the crescendo consists of either a single trill (Gs. demidoff) or a short sequence of trills (Gs. thom- Buzzy alarms asi), starting with an increase in pitch and amplitude Buzzy alarms are homologous in Galagoides, Galago (overtone crescendo) followed by repeated, insect-like, and the eastern dwarf galagos but have very different high-frequency clicks (Fig. 3). The call is typically structures in the three groups (Fig. 3). Buzzy alarms used as a gathering call emitted when animals leave are often the first indicator of the presence of an animal or return to their nests. Lesser galagos (Galago spp.) that has not yet been detected visually (FG, personal are repetitive callers. They have low-frequency met- observations). Animals emit several buzzy alarms that ronomic and tonal calls that are emitted throughout may precede or alternate with yaps. The call is bisyl- the night, indicating a territorial function. Homology labic, consisting of an initial high-frequency unit fol- between the loud calls of eastern dwarf galago species lowed by a highly modulated, lower-frequency screech. and Galagoides crescendo calls is difficult to establish, In western Galagoides spp., the buzz is extremely brief. but such homology with Galago repetitive calls is clear, In Galago spp., it is a brief, noisy, low-frequency cough- as they share a basic temporal structure of repeated like call (cho-ha). In the eastern dwarf galago species, units forming syllables. the buzz is a long screech peculiar to the group. The loud calls emitted by eastern dwarf galagos are so variable that they are difficult to characterize. The group could be called the ‘varied callers’ or ‘modu- Loud calls lated callers’, as their loud calls consist of repeated, Loud calls are far more variable between taxa than highly modulated units emitted at higher frequency anti-predatory calls. Each of the three small-bodied than Galago repetitive calls. Their function is also less genera emits a different kind of loud call associated clear, as they are given when animals leave or return

Figure 3. Sonograms of vocalizations emitted by small-bodied galagid species. Calls of Euoticus (Cameroon) and Galagoides granti (Tshanini, South Africa) were recorded by FG. All other sonograms were downloaded from the East African Primate Diversity and Conservation website (http://www.wildsolutions.nl/vocal-profiles).

to their sleeping sites, as well as throughout the night collections in the USA and Europe and identified when animals interact. The calls could hence be cat- seven probable Gs. rondoensis specimens in addi- egorized as long-distance contact calls adapted to tion to the type specimen held in the Natural History habitats that are generally drier than those of western Museum, London. Their identification was based on Galagoides, but wetter and more closed than Galago three factors: the consistent presence of a square M3 habitats (Génin et al., 2016). The specific diversity of with a very small hypocone (a very rare occurrence in this group still requires investigation, as only three other eastern dwarf galagos); collection locality (east call structures (i.e. scaling, rolling and incremental) of the Rift); and a disjunction between the completion have been described for at least five species. of the eruption of the permanent dentition and skull maturation. In most galagid genera, the attainment of adult body size occurs shortly after the complete eruption of the adult dentition. In the putative Gs. rondoen- MORPHOLOGICAL sis specimens we identified, animals with adult (and DIFFERENTIATION: NEW ANALYSES often worn) dentition had unfused cranial sutures and Morphological characterization of the eastern dwarf are likely to have continued to grow had their lives galagos has been complicated not only by the scarcity not been prematurely ended. Groves (2001) based his of exemplars of some species, but also by their strong assessment of Gs. rondoensis as the smallest living convergence with members of the western clade. In a galagid on the type specimen that had a body weight canonical variate morphometric analysis, the skulls of of 60 g, but animals trapped in the field may be 20–25 the type specimens of Gs. orinus and Gs. rondoensis g heavier (Andrew Perkin, personal communication). clustered with the western clade, contradicting their The type specimen has its permanent dentition, but genetic affinity to Gs. granti and Gs. zanzibaricus its morphology is juvenile, and fully grown members (Masters & Couette, 2015). In an attempt to resolve of this species are likely to be larger than Galagoides this contradiction, we searched through museum orinus adults.

Materials and methods used in the new morphometric analyses In order to investigate the morphological distinc- tiveness of the eastern dwarf galagos from other small-bodied galagids, a set of 12 linear craniodental measurements was taken from 610 galago specimens including western dwarf galagos (Gs. demidoff and Gs. thomasi, n = 322; see Masters & Couette, 2015 for specimen list), lesser galagos (Galago moholi, n = 150) and squirrel galagos (Sciurocheirus alleni, s.l., n = 58), plus specimens formerly identified as Gs. cocos, Gs. granti, Gs. orinus, Gs. rondoensis, Gs. udzungwensis and Gs. zanzibaricus (n = 80). Accession details of these specimens are listed in Table 1 of the supplementary data, and the institutions in which mensural data were collected are listed in the ‘Acknowledgements’ section. We followed the methodology of Masters & Couette (2015): measurements (Fig. 4; Table 1) were recorded using digital callipers, and the sample was composed only of specimens with fully erupted dentition. Raw data were size-adjusted using the Burnaby (1966) procedure that consists of extracting an isometric vector from the multivariate data set and back-projecting the values in a multivariate subspace orthogonal to this vector (Klingenberg, 1996). The geometric mean (GM) was computed using the isometric vector and served as a proxy for size. Thus, size (GM) and shape (size- corrected variables = shape variables) are considered Figure 4. Schematic depiction of an eastern dwarf galago independently through analysis of variance (ANOVA; skull showing the 12 craniodental measurements included size) or multivariate analysis of variance (MANOVA), in the multivariate morphometric analyses. Descriptions of principle component analysis (PCA) and canonical the variables are presented in Table 1.

Table 1. Cranial measurements used in the study (illustrated in Fig. 1)

Abbreviation Name Definition

SL Supraoccipital length From lambda to opisthion CH Cranial height From basioccipital–basisphenoid suture to the highest point of the braincase FL Frontal length From bregma to nasion IC Interorbital constriction Minimal distance between the inner margins of the orbits CTW Cheek teeth width Maximum width of right M1 PW Palate width Distance between labial margins of right and left P2 TSL Total skull length From prosthion to opisthocranion SnL Snout length From prosthion to nasion MW Mastoid width Distance between left and right mastoid processes TC Temporal constriction Minimum distance between left and right frontotemporals P Premaxilla Length of the premaxillary tube TCL Toothcomb length From the base to the tip of the incisors

variate analysis (log-transformed values of shape). We shape differences. The cranial morphology of Galagoides performed a between-group PCA (BGPCA; Mitteroecker individuals was clearly different from that of the Galago & Bookstein, 2011), which is a classic PCA based on the specimens, and the differences constituted the major mean values for each group with no regard for intra- variation along PC1. On this axis, all of the variables group variation. Specimens are then back-plotted in had similar loadings (values between −0.24 and 0.07) the morphospace by multiplying the morphological data except for premaxillary length, for which the loading matrix (log-transformed values of shape) by the coef- was very high (0.91); hence, the greater part of variation ficient of the BGPCA; the principle components (PCs) along PC1 was due to differences in the length of the tip are computed only on the intergroup variation rather of the muzzle. PC2 separated the genus Sciurocheirus than on a mix of intra- and intergroup variations. All (positive values) and the genera Galago and Galagoides statistics were performed with R 3.2.3. software (R Core (negative values). The variation along PC2 was mainly Team, 2015) and the packages ‘candisc’ (Friendly & Fox, structured by cheek tooth width (CTW), snout length 2015), ‘car’ (Fox & Weisberg, 2011), ‘geomorph’ (Adams & (SnL) and toothcomb length (TCL), with positive values; Otarola-Castillo, 2013) and ‘smatr’ (Warton et al., 2012). and temporal constriction (TC), supraoccipital length (SL) and mastoid width (MW), with negative values. The eastern dwarf galagos showed intermediate cranial morphologies and fell between Galago and Galagoides Results of the morphometric analyses on PC1 and between Sciurocheirus and the group com- MANOVA results attested to significant differences in posed of Galago and Galagoides on PC2. Although the cranial morphology among genera (Pillai’s trace = 1.84, three groups were clearly distinguished on PC1, they F = 86.09, d.f. = 33, P < 0.001). In the BGPCA, three PCs overlapped on PC2. The putative Gs. rondoensis speci- summed up the entire variation in our sample: PC1, PC2 mens were scattered in the space between the eastern and PC3 accounted for 88.9%, 9.91% and 1.19%, respec- dwarf species and Galagoides, and their variation in tively. The genera Galago, Galagoides and Sciurocheirus body size was evident (Fig. 5); despite our best efforts, it were well separated in the PC1 × PC2 morphospace, is possible that our sample included representatives of with no overlap except for some outlier specimens (Fig. more than one species. The Gs. orinus specimens formed 5). The presence of outliers and the degree of dispersion part of the main eastern dwarf cluster, although they evident in Fig. 5 may mean that some subadult skulls overlapped with some Gs. rondoensis specimens. were included, along with their correlated allometric Canonical discriminant analysis defined three significant canonical axes, accounting for 70.98%, 27.06% and 1.96% of interclass variation (Fig. 6). The variable Premaxilla (P) contributed the main discrimination along the first axis. The four genera were well indi- vidualized on the first two axes, with high percentages of correct classification: 100% for Galago, 98.14% for Galagoides, 91.3% for the eastern dwarf galagos and 86% for Sciurocheirus. As is evident in visual compari- sons of skulls, the elongation of the P is greatest in Galagoides, smaller in the eastern dwarf galagos and smallest in Galago [Tukey’s honest significant difference (HSD) post hoc test P-values < 0.01 among these genera], but the difference in premaxillary length between the eastern dwarf galagos and Sciurocheirus was not significant. The variables with highest loading on the second axis were total skull length (TSL), SnL and CTW. The eastern dwarf galagos differed significantly in SnL from Galago and Sciurocheirus, but not from Galagoides. All of the genera differed significantly in CTW, with values increasing from Galago through Galagoides to the eastern dwarfs and finally Figure 5. Between-group principle component analysis Sciurocheirus, the large bunodont molars of which (BGPCA) calculated on the 12 shape variables. Crosses indi- evince its affinity to Otolemur spp. A similar trend is cate the mean values of each group that defined the principle noticeable for TSL measurements, with the smallest component axes to analyse intergroup variation. Specimen values in Galagoides, increasing in Galago and the data were back-projected in this space. Specimens of the two eastern dwarfs and with Sciurocheirus having the smallest eastern taxa, orinus and rondoensis, are indicated. longest skulls. As in the BGPCA, the Gs. rondoensis

Figure 6. Canonical variate analysis of the 12 shape vari- Figure 7. Allometric trajectories for each genus described ables. Crosses indicate the centroid of each group. The first by the linear regression of PC1 against the log-transformed two roots illustrate significant differences in skull shape centroid size. The allometric patterns are different among among genera. Specimens of the two smallest eastern taxa, genera. Unlike the other genera, the eastern dwarf galago orinus and rondoensis, are indicated. taxa do not show significant allometry. Specimens of the two smallest eastern taxa, orinus and rondoensis, are indicated. specimens occupied the morphospace between the all other genera: the allometric slopes of the variables eastern dwarf galagos and Galagoides, while Gs. orinus SL, cranial height, frontal length, CTW, palate width, was more closely grouped with the eastern dwarf spe- MW, TC and P were all significantly different. The east- cies. Specimens of Gs. rondoensis and Gs. orinus show ern dwarf galagos differed in slope from Galago for var- intermediate morphology and overlap with eastern iables SL and CTW and from Galagoides for variables dwarf galagos and specimens of the genus Galagoides. interorbital constriction (IC), CTW, TSL and P. An ANOVA of skull size repeats the pattern shown Sciurocheirus is hence clearly differentiated in both by TSL (P-value < 0.001 and all Tukey’s HSD multi- size and shape. Comparing the three smaller-sized gen- ple comparison of mean P-values below 0.001). In order era, our multivariate analyses indicated marked differ- to test the relationship of size (GM) and shape (logged ences in cranial shape among them. From a univariate size-corrected variable), we performed a multivariate perspective, the eastern dwarf group differed mainly regression considering the effect of size on shape, genus in SL (intermediate between Galago and Galagoides), and the interaction between size and genus. We used a IC, CTW and TSL (higher values in the eastern dwarf Type II ANOVA to test each term of the linear model. group). These morphometric differences reinforce our Size, genus and the interaction had a significant effect proposal to distinguish the eastern dwarf galagos from on shape with P-values below 0.001, attesting that Galago and Galagoides at the generic level. shape variation is explained by size variation (allometry). The common allometry, that is the proportion of shape explained by size across the entire sample, was SYSTEMATICS 77.7%, but considering the allometric vectors for each genus yielded much lower values: size accounted for Paragalago gen. nov. 15.1% of shape variation in Galago, 20% in Galagoides, 13.8% in the eastern dwarfs and 8.7% in Sciurocheirus. http://zoobank.org/urn:lsid:zoobank.org:act: Pairwise comparison of multivariate allometric pat- 4B5DD0A6-BB35-4C9E-B292-AA69A90D6431 terns demonstrated significant differences between the eastern dwarfs and Galago (P-value of angle between Type species: Galago zanzibaricus Matschie, 1893. allometric vectors = 0.0428), Galagoides (P = 0.019) and Sciurocheirus (P = 0.014; Fig. 7). With respect to Included species: Galago granti Thomas & Wroughton, univariate differences in allometries among genera, 1907; Galago cocos Heller, 1912; Galago demidovii Sciurocheirus presented a very different pattern from orinus Lawrence & Washburn, 1936; Galagoides

udzungwensis Honess, 1996; Galagoides rondoensis outline a broad parietal plate over the orbits that Honess, 1996. narrows posteriorly. The colour of the dorsal pelage is drab brown to Diagnosis: Medium- to small-sized galagos (60–250 cinnamon with varying degrees of rufous wash; outer g), overlapping in size with Galago spp. and notably surfaces of limbs are similar to dorsum in coloura- smaller than Sciurocheirus, Euoticus and Otolemur tion. Individual hairs are slate grey near the root, spp. Two species (Paragalago orinus and Paragalago contributing to the overall dark colouration. Hairs rondoensis) show convergence in shape and size with on ventrum and inner surfaces of limbs also have Galagoides spp. Cranium is ovoid in shape, narrowing grey roots but cream buff to yellow buff tips, and the posteriorly, so that the pneumatized mastoids throat may be yellowish (Groves, 2001). The ears are protrude. Premaxillaries protracted into a short tube dark brown to black, depending on the species, and that extends beyond lower jaw, as in Galagoides and the tail varies from rufous brown to chocolate or even Sciurocheirus; the tubular extension in Paragalago is black. Paragalago granti and P. orinus have a darker intermediate in length between the premaxillary tubes tail tip. The cream to white nose stripe is emphasized of the smaller and larger taxa. Anterior upper premolar by dark brown to black eye rings. Mature males of (P2) double-rooted, slender, but distally trenchant, all species have unidentate penile spines (Perkin, as in Galagoides, not caniniform as in Euoticus and 2007). Species of Paragalago show behavioural dif- some Galago spp. Upper posterior premolars (P4s) are ferences that distinguish them in the field from both slightly larger than upper posterior molars (M3s) in Galagoides and Galago taxa. Eastern dwarf galagos most Paragalago specimens examined. In Galagoides tend to leap more often than Galagoides, but not as M3 is either larger or equivalent in size to P4, while frequently or extensively as Galago spp. Moreover, in Galago M3 is much reduced. In Paragalago spp., the three genera can be readily distinguished by the M3 hypocone is absent or minute but commonly vocalizations that differ in structure, in context and observed in Galagoides spp. Coronoid processes probably in function. delicate and curved, extending almost as far back as glenoid process, as in Sciurocheirus and Galagoides, Notes: The new genus embraces several taxa originally not flattened and foreshortened, as in Galago and allied with lesser or dwarf galagos, depending on body Euoticus. size. Paragalago zanzibaricus was described by Paul Matschie (1893) as a pale cinnamon-coloured lesser Distribution: east of the Great African Rift. galago from western Zanzibar, although the species also occurs on the Tanzanian mainland (see Fig. 2). Description: The snout is longer than in Galago, chiefly A recent conservation risk assessment conducted by because premaxillaries extend well beyond the lower the Primate Specialist Group of the International jaw, although not to the degree seen in Galagoides. The Union for the Conservation of Nature considered facial profile is distinctly concave (Schwarz, 1931) as in populations on small islands to be particularly Galagoides and Sciurocheirus, not straight or slightly vulnerable and deserving of subspecific recognition convex as in Galago. Canines are slender. Anterior for the purpose of conservation monitoring. The palatal foramina intrude between medial upper Zanzibar population of dwarf galagos was hence incisors, as in most galagid taxa. P4s fully molarized as designated as the subspecies P. z. zanzibaricus, while in all crown galagids. In most Paragalago specimens the mainland representatives of this species were examined, the M3 had no hypocone, although a minute classified as P. z. udzungwensis. Preliminary genetic hypocone was present in some specimens from the studies of mainland and island populations (Pozzi, Rondo Forest (probably P. rondoensis). The degree of unpublished data) support their conspecific identity, basicranial flexion is moderate, as seen in Galagoides, but a more extensive comparison is necessary to Otolemur and Sciurocheirus, not markedly flexed as confirm this. in Euoticus and in Galago. Cranial shape is oblong Paragalago cocos, which is morphologically indistin- as in Galagoides and Sciurocheirus, not globular guishable from P. zanzibaricus, was described by Heller as in Galago and Euoticus. Postorbital bars are (1912) from the Kenyan mainland. Paragalago granti, generally slender, lacking the flanges sometimes seen with a type locality in southern Mozambique, has the in Euoticus, Galago and even Galagoides, usually in largest geographical range among representatives of the genus, extending from the north-east of South older specimens. Lower anterior premolars (P2) are partially procumbent, but not to the same degree as Africa throughout Mozambique (and possibly parts of the toothcomb, and never erect, as usually seen in Malawi, where it has been referred to under the rubric male Galagoides (Masters & Couette, 2015). Parietal Galagoides nyasae Elliot, 1907; Grubb et al., 2003) into muscle scars/crests on either side of the medial suture southern Tanzania. The type and only known skin of

Galago mertensi Frade, 1924, was collected at a local- USA); National Museum of Scotland (Edinburgh, ity not far west of the type locality of P. granti and has, UK); Naturmuseum Senckenberg (Frankfurt-am- rightly or wrongly, been subsumed under this species Main, Germany); and Zoologisches Forschungmuseum (Schwarz, 1931). Alexander Koenig (Bonn, Germany). We express The two smallest members of the genus, P. orinus our gratitude to two reviewers whose suggestions and P. rondoensis, are the most recent members of the improved the final text significantly and to the col- eastern dwarf clade to have been accorded full species leagues who have advised, assisted and encouraged status. Paragalago orinus is a montane endemic and us, particularly Simon Bearder, Iris Dröscher, Paula occurs within a restricted habitat at high altitude in Jenkins, Nokuthula Kom, John Oates, Andrew Perkin, the Udzungwa and Uluguru mountains of Tanzania. 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SUPPORTING INFORMATION Additional Supporting Information may be found in the online version of this article at the publisher’s web-site: Table S1. Eastern dwarf specimens included in the morphometric analysis of skulls.

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