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Zitteliana B 32 (2014) 175

Behavioural phylogeny of

Pierre Deleporte1* & Henri Cap2

 Zitteliana B 32, 175 – 184 1Université de Rennes 1, CNRS, UMR6552 EthoS, Station Biologique, 35380 Paimpont, France.  München, 31.12.2014 2Muséum d’Histoire Naturelle de Toulouse, 31000 Toulouse, France.

 Manuscript received *Author for correspondence and reprint requests; E-mail: [email protected] 30.04.2014; revision accepted 02.10.2014

 ISSN 1612 - 4138

Abstract

In this article, we examine the possible contribution of behavioural studies to the determination of phylogenetic relationships within the Bovidae. First, we revisit the general arguments concerning the use of behavioural traits as phylogenetic characters; then we present our first attempt at reconstructing the phylogeny of Bovidae based on behavioural data taken from the literature. Despite the limited number of characters used, several clades of low hierarchical levels are supported by this phylogenetic analysis, in much the same manner as by morphological and molecular ones. Several characters linked to male sexual behaviour appear to be among the more informative ones. Key words: Phylogeny, behaviour, Bovidae, methods.

1. Introduction tions; however, basing phylogenetic inference upon behavioural traits is not universally accepted. Early Methods for phylogenetic inference are under- ethologists had no such reluctance. The founders of going tremendous changes with the advent of mo- behavioural sciences were keen to demonstrate that lecular approaches. This does not mean that the behavioural characters, much like morphological more traditional morphological and behavioural ones, could provide relevant taxonomic evidence. approaches should now be completely neglected. Even if genuine and explicit phylogenetic methods Both have proved successful in unraveling some well were not immediately implemented, a taxonomic supported phylogenetic relationships. In the ongoing work like that of Lorenz (1941) on anatid birds, later debates about the phylogeny of , we be- developed by Johnsgard (1961) under the name of lieve that behavioural characters could play a role, evolutionary relationships of Anatidae, produced de provided that more extensive and detailed work is facto phylogenetic patterns based on behavioural developed in this direction. Given the lasting con- characters, largely in accordance with morphology- troversies about the merits of different kinds of char- based phylogenetic relationships (Irwin 1996). Later acters for phylogenetic inference, we first review the on, many ethologists focused mainly on epigenetic classic arguments for and against the use of behavi- processes driving the emergence of the more pla- oural characters for phylogenetic inference. We then stic aspects of behaviour. More recently, there has propose a preliminary phylogenetic analysis of Bovi- been a resurgence of interest in comparative etho- dae based on behavioural characters collected from logy due to theoretical developments in the study of the literature. behavioural evolution (like sociobiology) and metho- dological developments (phylogenetic systematics and computer-assisted inference methods). These 2. Behavioural phylogenetics: advancements have allowed comparative ethology methodological considerations to take an explicit phylogenetic perspective. In this context, differing opinions have been expressed re- The use of behavioural characters in phylogene- garding the possible use of behavioural characters tics is still a controversial topic. Mapping these char- in phylogenetic inference. Atz (1970) stands among acters on a phylogeny independently inferred from the radical opponents, negating the possibility of morphological or molecular characters to study the homologizing behavioural traits among different evolution of behaviour does not raise many objec- , limiting the focus to only morphological and Zitteliana B 32 (2014) 176 physiological traits. However, Atz (1970) concedes leged high plasticity of behavioral traits. Of course that among the “most convincing examples of ho- relevant phylogenetic characters are supposed to be mologous behavior” are the “patterns of locomotor heritable, and not just culturally or environmental- activities that are found in a single group of related ly acquired and modified. Hence plastic behaviors, species and in all the members of the group. Not to or the plastic parts of otherwise stereotyped beha- conclude that such behavior was also practiced by vioral sequences, should be identified. This can be the common ancestor […] would violate the principle done through careful and extensive observations. of parsimony.” Hence, despite his reticence, Atz ac- Ideally, individuals and groups of individuals of the cepted to consider uniquely derived and unreversed different species should be observed under varying characters as homologies, which finally appears as a developmental and environmental contexts, when conservative application of the ‘maximum parsimo- some epigenetic plasticity is suspected. Serial com- ny’ principle regularly used in phylogenetics. On the parative experiments using many individuals in con- other hand, Wenzel (1992) developed a detailed and trolled contexts are tractable in easily bred species balanced argument in favor of the use of behaviou- (for example insects, Legendre et al. 2008, 2014). Of ral characters for phylogenetic inference. He listed course this is more difficult for free ranging and rare 23 authors who generated phylogenies from behavi- or cryptic . Extensive observational studies of oural data. De Queiroz & Wimberger (1993) showed, behavior under comparable conditions are very de- from bibliographical analysis, that behavioural char- manding, but this is a practical, not a theoretical limit. acters were no more homoplastic than morphologi- Concern has been raised about using behavioural cal characters. characters for phylogenetic inference and then de- Without going through a detailed analysis, some scribing the evolution of these characters based on arguments need to be made. The question of ho- the reconstructed phylogeny: this should allegedly mology assessment for behavioural characters is be avoided to escape the flaw of circular reasoning; rather straightforward. Basically, the classical ho- e.g. Brooks & McLennan (1991) raised this point as mology criteria – position, connection by intermedi- a “cardinal rule”. In fact, this would be true only if ates, and special quality – are applicable to behavi- one would use just a single behavioural character our, although in some specific ways (Wenzel 1992). for phylogeny inference, and then draw an optimal Ever since early ethological approaches, position is evolutionary scenario for the same character from deduced through the succession of behavioural the phylogenetic topology. When many phylogene- items in behavioural sequences. Molecular phylo- tic characters are used and the optimal phylogene- geneticists proceed in a similar way when using the tic topology is identified through overall congruence position of base pairs in otherwise “aligned” homo- among character distributions, no tautology or vi- logous sequences of DNA. Behavioural sequences cious circular reasoning is ever involved (Deleporte may be both much shorter and much more diverse 1993; Grandcolas et al. 2001). Brooks & McLennan in their components. Classical sequence analysis (2002) came to the same conclusion: “Use all availa- dealt with complex stereotyped behavioural pat- ble evidence to construct your phylogenetic hypo- terns. More recently, analyses of behavioural se- thesis, but be sure that the phylogenetic tree being quences within social interactions of insects have used to investigate the evolution of trait x depicts used elementary successions of specific behavioural relationships that are maintained when trait x is ex- actions, with convincing phylogenetic results (suc- cluded from the analysis”. cessive event-pairing method, Legendre et al. 2008, Phylogenetic inference is an exercise in the “plau- 2014). Connection by intermediates is used for dia- sible narrative” (Clauss & Rössner 2014) for which gnosing variants of a behavioural pattern as likely all relevant evidence must be used (in the broadest homologous character states of a unique behaviou- sense of all relevant knowledge; i.e. not just all the ral character progressively modified through a con- characters (or “all the data”) but also all we can know tinuous evolution in closely related taxa. Secondary about them - Lecointre & Deleporte (2005). Traits of plotting on the phylogeny will tell the optimal evolu- dubious homology should be avoided (e.g. Grandco- tionary scenario for the character, but the necessary las et al. 2011), but all valid, informative characters a priori homology assessment is done through direct should be used. There is no reason to discard any po- comparison of behavioural variants. Special quality tentially informative evidence. Restricting evolution- is generally considered as the more useful criterion, ary studies of behavioural characters to plotting particularly for highly diverse kinds of behavioural them on an independent phylogeny hardly makes traits, hence limiting the risks of misleading homo- sense, because the criteria for inferring an optimal plasy. This criterion can be augmented with conside- evolutionary scenario are the same as those for se- ration of the function of behaviour, via the analysis of lecting phylogenetic characters in the first place: i.e. its context of expression, but function alone is hardly reliability of their primary homology. Whatever kind usable given the range of possible ways to fulfill a of characters is concerned; when a character is valid similar function. for evolutionary scenario optimization, it is also valid A common objection against the use of behavi- for taking part in the data matrix for phylogenetic in- oral characters in phylogenetic inference is the al- ference (Grandcolas et al. 2001). Zitteliana B 32 (2014) 177

Figure 1: (a) Phylogenetic topology (ML) of Bovidae inferred from mtDNA (Hassanin et al. 2012). (b) Phylogenetic topology (MP) of Bovi- dae inferred from morphology and behaviour (Vrba & Schaller 2000).

A last important question is how to combine dif- 3. Behavioural phylogeny of Bovidae ferent kinds of characters for phylogenetic inference. Ideally, biologists should understand the principles of Bovidae is the most diversified family of the order character evolution and use this background know- Cetartiodactyla (species numbers vary from ≈ 142 ledge to devise models for the analysis of different to ≈ 300 depending on the species concept used). kinds of characters. Molecular analyses regularly im- Recent molecular studies have reached a consen- plement explicit models of character change, required sus with morphological approaches at higher phy- in maximum likelihood approaches. In morphological logenetic levels (Hassanin et al. 2012), but several and behavioural phylogenetics, we tend to use equal relationships remain unresolved when compared to “weights”, “costs” or probabilities of change for all the results of the combined morphological and be- characters, largely because we do not know how havioural phylogenetic analysis by Vrba & Schaller to determine relative weights for the alternatives. It (2000). Both topologies are presented in Fig. 1. In must be noted that “equal weights” for any char-acter this study, we will first describe the taxonomic dis- transformation in maximum parsimony phylogeny tribution of diverse behavioural characters in rumi- inference is not an absence of a model, but a parti- nants, and then describe how comparative etholo- cular evolutionary model (coined as NCM - for “No gists may derive patterns of behavioural evolution Common Mechanism” - by Tuffley & Steel 1997). Per- without a specific phylogenetic reference. Finally, we forming separate phylogenetic analyses for different will use these characters for a tentative phylogenetic kinds of characters does not really solve the problem, inference based solely on behavioural characters. because the question will remain of how to balance the contribution of the different tentatively inferred 3.1 Data sources and methods phylogenies. By this somewhat pessimistic observati- on, we simply want to stress that, in the present state 3.1.1 Taxa and character sampling of biological knowledge, any phylogenetic inference should be taken very cautiously, given the risk of over- In this study, 42 bovid taxa were considered (Tab. estimating the resolution of the phylogenetic topology. 1). We analyzed the complete behavioural data set Fortunately, we can be rather confident in the histori- studied by Walther (1974), using his tables and addi- cal accuracy of the clades most strongly supported tional data from the text of the same chapter. Walther by different sources of evidence, assuming that these classed the 39 behavioural characters in three cate- inferences would resist some range of approximation gories: threat displays (postures, 12 characters), do- in character coding and evolutionary models. minance postures expressed in hostile encounters (9 In the following analysis, we will adhere to a clas- characters) and patterns of male courtship displays sic, uniformly-weighted, parsimony approach, be- (18 characters). These characters are listed and de- cause appropriate weighting schemes for alterna- fined in Tab. 2. In the corresponding data matrix for tives are not known. phylogenetic analysis (Tab. 3), the absence or pre- Zitteliana B 32 (2014) 178

Table 1: Taxa analyzed in this study (bibliographic source: Walther, Table 2: Male and female behavioural characters (bibliographic 1974). source: Walther 1974). Taxon Common name Threat displays

Bovinae 1) Pawing the ground (without urination or defecation) in hostile : encounters. taurus cow 2) Nose (vertically) upward posture in females. Bos gaurus 3) Symbolic snapping in females. bison 4) Rising on hind legs in hostile encounters. : 5) Dropping down onto knees. Boselaphus tragocamelus 6) Lateral head-shaking (like in negation). : 7) Symbolic butting and/or head nodding (like humans in scriptus bushbuck affirmation). Tragelaphus spekei 8) Downward sweep of head and horns. Tragelaphus angasi 9) Medial presentation of horns. Tragelaphus imberbis esser 10) High presentation of horns. Tragelaphus strepsiceros 11) Low presentation of horns. 12) Head low posture. Dominance displays in hostile encounters Cephalophini: Broadside displays: Cephalophus nigrifrons black fronted 13) Arched-neck posture. : 14) Head-low posture. campestris 15) Head-and-neck-stretched-forward posture. Madoqua kirki Kirk’s dikdik 16) Lifted-head posture. Gazella gazella mountain 17) Erected posture. Gazella dorcas Frontal displays: Gazella thomsoni Thomson’s gazelle = thomsoni Gazella subgutturosa 18) Head-turn (approximately 90°). Gazella soemmerringi Soemmerring´s gazelle = 19) Erected posture. soemmerringi 20) Lifted-head posture. Gazella granti Grant’s gazelle = Nanger granti 21) Head-and-neck-stretched-forward posture. Litocranius walleri Male courtship displays Antilope cervicapra Indian Broadside displays: Oreotragini: 22) Head-low posture. Oreotragus oreotragus 23) Head-and-neck-stretched-forward posture. Alcelaphini: 24) Lifted-head posture. Connochaetes taurinus blue 25) Erected posture. Alcelaphus buselaphus Postures in following the female: lunatus 26) Head-turn (approximately at right angle). Damaliscus pygargus 27) Erected posture. Hippotragini: 28) Lifted-head posture. Oryx gazella 29) Head-and-neck-stretched-forward posture. niger sable 30) Arched-neck posture. Hippotragus equinus 31) Head-low posture. Reduncini: ellipsiprymnus Laufschlag: Kobus kob 32) Kick with the foreleg combined with head-and-neck- Kobus leche stretched-forward posture. Kobus megaceros 33) Kick with the foreleg in normal or slightly erected posture. Redunca arundinum southern 34) Kick with the foreleg combined with lifted-head posture. Aepycerotini: Mounting postures: Aepyceros melampus 35) Mounting with chest, chin and sometimes also throat on the Caprini: female’s back. ammon 36) Mounting with chest and nose (vertically) on the female’s back. Ovis canadensis 37) Mounting with chest on the female’s back, head and neck Ammotragus lervia leaning forward but not touching the female’s body. ibex 38) Mounting with chest on the female’s back, neck erected. Capra falconeri 39) Mounting in standing or walking behind the female, chest not Oreamnos americanus mountain touching the female’s back. rupicapra Alpine Zitteliana B 32 (2014) 179 Table 3: Data matrix of behavioural characters in the studied taxa. Coding: 0 = character absent, 1 = character present, ? = undocumented.

sence of characters are coded 0 and 1 respectively, Reduncini (except Kobus leche). This behaviour is while undocumented characters are noted “?”. In also found in all other families. It may be a order to simplify the phylogenetic resolution, we plesiomorphic feature linked to an ancestral pursuit coded as present the characters that Walther (1974) deterrent signal expressed by a solitary, territorial considered as only possibly present. We considered species in response to the perception of a predator that behaviour occasionally observed may consti- or a conspecific individual entering the territory. tute phylogenetically informative data. Of course this As far as the Reduncini are concerned, it is in- character coding should be reevaluated in further teresting to note that none of the territorial water- studies. buck species mark their territory by establishing dung piles or with preorbital gland secretion (Walther 3.1.2 Behavioural phylogenetic analysis 1974). This could indicate a less robust expression of territoriality in these species, similar to the Capri- The behavioural data matrix (Tab. 3) was analyzed ni, Tragelaphini and Boselaphini. The only surprising by maximum parsimony under equal weights, using appearance for this character is in the Bovini, not ty- PAUP 4.0 pically considered territorial species, yet expressing this behaviour. This is in contrast to Aepyceros me- 4. Results lampus and Antilope cervicapra, territorial species that do not express this behaviour. 4.1 Taxonomic distribution of the 2) Nose vertically upward posture in females: pre- behavioural characters sent in Tragelaphini and Boselaphini, it could be syn- apomorphic for these taxa although several other 4.1.1 Threat displays Antilopinae species seem to have acquired this char- acter by convergence (Litocranius walleri, Nanger 1) Pawing the ground: found in most bovid taxa: granti, Kobus ellipsiprymnus and K. megaceros). exceptions include Tragelaphini, Boselaphini, Aepy- 3) Symbolic snapping in females: present in Tra- cerotini, Antilope cervicapra, most of the Caprini (ex- gelaphini and Boselaphini, could be synapomorphic cept Ovis ammon and Oreamnos americanus) and for these taxa while Antilope cervicapra, Oreotragus Zitteliana B 32 (2014) 180 oreotragus, Kobus ellipsiprymnus and Cephalophus 15) Head-and-neck-stretched-forward posture: nigrifrons may have acquired this character by con- present in Tragelaphus species and Boselaphus and vergence. This ancestral behaviour is also seen in by convergence in one Gazella and Damaliscus spe- other ruminant, nonruminant cetartiodactyls and cies. It appears to be highly homoplastic. even in perissodactyls. It may be a relict behaviour, 16) Lifted-head posture: present in most Trage- retained in non-territorial species such as Tragela- laphus species and Boselaphus and by convergence phini and Boselaphini and in some territorial ones in several Antilopinae species. such as the four Antilopinae noted previously. 17) Erected posture: present in all Antilopinae ex- 4) Rising on hind legs in hostile encounters: pre- cept most of Caprini, Gazella dorcas and Eudorcas sent in Caprini and seems to be synapomorphic for thomsoni. Also present by convergence in Trage- these taxa. Several other species express this be- laphus angasi and Taurotragus oryx. This character haviour (Nanger granti, Aepyceros melampus, Bose- seems to be a synapomorphy of Antilopinae, lost in laphus tragocamelus, Damaliscus lunatus). some species. 5) Dropping down onto knees: present in all Hip- potragini and Alcelaphini species, and also by con- 4.1.2.2 Frontal displays vergence in isolated species (Bos taurus and Bose- laphus tragocamelus for and Kobus leche 18) Head-turn (approximately 90°): present in all for Antilopinae). bovid species with some notable exceptions: Bos 6) Head-shaking (like humans in negation): pre- gaurus, most Tragelaphus species, Boselaphus, and sent in most of Bovinae (except Bos taurus, Bose- several species within Antilopinae. This character laphus and Taurotragus) and in ten different Antilopi- seems to be symplesiomorphic for bovids. nae species but without any tribal association which 19) Erected posture: present in all bovid species may indicate a high level of homoplasy. except most species of Tragelaphus, Boselaphus, 7) Symbolic butting and/or head nodding (like several species within the Caprini and most species humans in affirmation): present in most of Bovinae of Gazella. This character seems to be symplesio- (except Bos taurus and Boselaphus), Hippotragini morphic for bovids, its loss being synapomorphic for (except Hippotragus niger), Alcelaphini and several the clades mentioned. other Antilopinae species. Like the latter character, 20) Lifted-head posture: present in several tribes this feature seems to be homoplastic. including the Antilopini, Caprini, and Reduncini. It is 8) Downward sweep of head and horns: present also found in several species of Tragelaphus and An- in several species of different lineages. As with char- tilopinae, perhaps through convergence. It appears acter 6 and 7, it seems to be highly homoplastic. to be highly homoplastic. 9) Medial presentation of horns: present in all bo- 21) Head-and-neck-stretched-forward posture: vid species except Bos gaurus, Bison bison, Oryx present in most species of Tragelaphus and Bose- gazella and Hippotragus equinus. This character laphus. It is also found in several species of Antilopi- seems to be symplesiomorphic for bovid species. nae, perhaps through convergence. 10) High presentation of horns: present in all Hippotragini and Gazella species (except G. soem- 4.1.3 Male courtship displays merringi), and also by convergence in other species (Tragelaphus goesi, Kobus ellipsiprymnus and Ovis 4.1.3.1 Broadside displays ammon). 11) Low presentation of horns: present in all bo- 22) Head-low posture: present only in three spe- vid species except Bison bison, several Antilopinae cies of Bovinae: Bison bison, Tragelaphus angasi species and a majority of the Caprini. This character and T. strepsiceros, possibly convergent. seems to be plesiomorphic for bovid species. 23) Head-and-neck-stretched-forward posture: 12) Head low posture: present in all bovid species present in all Tragelaphini, Boselaphini and Bovini except Bison bison, several Antilopinae species and (except Bos taurus). It seems to be synapomorphic again a majority of Caprini. This character seems to for these taxa. Several other clades have acquired be a bovid symplesiomorphy. this character, perhaps by convergence (in Gazella, Alcelaphini, and twice in Caprini). 4.1.2 Dominance displays in hostile encounters 24) Lifted-head posture: present in all Bovini and also by convergence in different tribes. 4.1.2.1 Broadside displays 25) Erected posture: present in several bovid spe- cies. It seems highly homoplastic. 13) Arched-neck posture: present in all bovid spe- cies except most of the Tragelaphini and Caprini, it 4.1.3.2 Postures in following the female seems to be a bovid symplesiomorphy. 14) Head-low posture: present in all Bovini and Al- 26) Head-turn (approximately at right angle): pre- celaphini species, and also likely by convergence in sent in most of Tragelaphini and Boselaphini and in scattered species. several bovid species. It seems highly homoplastic. Zitteliana B 32 (2014) 181 27) Erected posture: present in all bovids except This behaviour, also expressed by , gi- in Bovini and Alcelaphini. This character seems to be raffids and moschids, seems plesiomorphic for Bo- a bovid symplesiomorphy, lost in the two mentioned vidae. clades. 39) Mounting in standing or walking behind the fe- 28) Lifted-head posture: present in Nanger, all male, chest not touching the female’s back: present Gazella and all Bovini species. It appears in several in all Antilopini, Madoqua, Litocranius and Raphice- other disparate species, perhaps through conver- rus (hence some Antilopini also present posture 38 gence. with chest on female’s back). 29) Head-and-neck-stretched-forward posture: present in all bovids with the following exceptions: 4.2 Behavioural phylogenetic patterns Hippotragini and two species from the Bovini. This character seems to be a bovid symplesiomorphy, The phylogenetic tree generated from the maxi- lost in the two mentioned clades. mum parsimony analysis of all behavioural char- 30) Arched-neck posture: present only in three acters with equal weights is presented in Fig. 2. Antilopinae species: Gazella gazella and two species Only one alternative equiparsimonious topology was of Damaliscus. found. The consensus of these two trees is largely 31) Head-low posture: present only in two Trage- unresolved, and there is no Bremer support or si- laphus species, and Kobus megaceros. gnificant bootstrap support for the clades (very low CI and RI, only 52 % bootstrap support for Trage- 4.1.3.3 Laufschlag laphini). Hence, in its present state, our tentative behaviour-based phylogeny should not be consi- 32) Kick with the foreleg combined with head- dered as challenging current molecular or morpho- and-neck-stretched-forward posture: present in all logical phylogenetic analyses. In Fig. 2, the clade Caprini (except Ammotragus) and two Gazella. (Oreotragus, Kobus ellipsiprymnus, Ovis, Capra) 33) Kick with the foreleg in normal or slight- joins with Ammotragus lervia, Redunca arundinum, ly erected posture: absent in all Bovinae, present Oreamnos americanus and two species of Kobus. in most of Antilopinae tribes except Alcelaphini. It In the alternative tree, the clade (Oreotragus, Kobus seems to constitute a synapomorphy of Antilopinae. ellipsiprymnus, Ovis, Capra) is positioned as sister 34) Kick with the foreleg combined with lifted- group of the clade including both Kobus leche and head posture: present only in Nanger granti, Eudor- Tragelaphus, the remainder of the topology being cas thomsoni, Antilope and Litocranius. otherwise unchanged. We comment only on the first topology because it shows a more plausible arran- 4.1.3.4 Mounting postures gement of Caprini relative to previous morphological and molecular analyses (e.g. Vrba & Schaller 2000; 35) Mounting with chest, chin and sometimes also Hassanin et al. 2012). throat on the female’s back: present in all species of Bovinae. This behaviour seems to be an unam- Node 1 biguous synapomorphy for this clade if compared to the mounting postures in outgroups: male Cer- - Bovidae: the ancestral bovid ethotype appears vidae mount with the chest and nose vertically on to have exhibited the following behaviour: paw- the female’s back (Dubost 1971), whereas Antiloca- ing the ground (character 1); presentation of horns pridae (O’Gara 1990), (Green 1985) and high and low (9 and 11) and head low posture (12) (Cap 2006) are characterized by mounting in threat displays; arched-neck posture (13) in do- with chest on the female’s back, head more or less minance broadside displays; head-turn (18) and erected. erected posture (19) in dominance frontal displays; 36) Mounting with chest and nose (vertically) on head-and-neck-stretched-forward posture (29) during the female’s back: present in all Alcelaphini species male courtship displays in following the female; and (synapomorphy) and possibly by convergence in mounting with chest, chin and sometimes also throat Cephalophus, Oreamnos and Boselaphus tragoca- on the female’s back (35). The latter behaviour could melus. These species share this trait with all cervids also be an apomorphy of Bovinae, shared by Bovini, (plesiomorphic or convergent). Tragelaphini and Boselaphini (this group is not mo- 37) Mounting with chest on the female’s back, nophyletic in this tree). head and neck leaning forward but not touching the - Bovini: Several characters are shared by spe- female’s body: present in two Kobus species, and cies within the Bovini (Bos taurus, B. gaurus and Bi- possibly by convergence in Rupicapra and Cepha- son bison): Head-low posture (14) during broadside lophus. dominance displays which is also present by con- 38) Mounting with chest on the female’s back, vergence in Alcelaphini and several disparate Anti- neck erected: absent in Bovinae (synapomorphy) lopinae species. Lifted-head posture in broadside and present in most of Antilopinae except Alcelaphi- displays (24) and in following the female (28) during ni, two Gazella species, Cephalophus, and Antilope. male courtship are behaviours also present in this Zitteliana B 32 (2014) 182

Figure 2: Most parsimonious tree supported by behavioural data from Walther (1974). Tree length = 215 steps; CI = 0.18; RI = 0.54. Each node labeled with a number refers to descriptions of synapomorphies in the text. group. These are also found in other tribes. (36), present also in Cephalophus, Oreamnos and Boselaphus. Node 2 Node 4 Antilopinae + (Tragelaphini, Boselaphini): This group is characterized by erected posture in domi- This group contains Tragelaphini, Boselaphini, nance broadside displays (17), a character found in a and all Antilopinae tribes except Alcelaphini. It is majority of the Antilopinae studied. It is also present characterized by kick with the foreleg in normal or in Tragelaphus angasi and Taurotragus oryx perhaps slightly erected posture (33), except for Tragelaphini through convergence. The latter species also share and Boselaphini; this character is not found in any the same reversions of lifted-head posture in broad- Bovinae. Likewise, this group displays mounting with side displays (24) and in following the female (28), chest on the female’s back, neck erected (38), again but they do not mount with chest, chin and some- absent in the Bovinae (Bovini, Tragelaphini, Bose- times throat on the female’s back (35). laphini). This grouping at node 4 is in conflict with most molecular-based phylogenies (Hassanin et al. Node 3 2012), according to which it would appear as poly- phyletic, linking parts of the Antilopinae to parts of Alcelaphini: head-low posture (14) during broad- the Bovinae. These ‘unifying’ behavioural characters side dominance displays appears to be an informa- may simply be synapomorphies of most Antilopinae; tive character. This character is also present in all Tragelaphini and Boselaphini being misplaced due Bovini and in a few other isolated species possibly to convergence in several highly homoplastic char- due to convergence. Head-and-neck-stretched-for- acters (see nodes 10 and 11 below). ward posture (23) during male courtship broadside displays is similar in its distribution. The only unam- Node 5 biguous synapomorphy in this group is mounting with chest and nose (vertically) on the female’s back The same group as the previous one without Ko- Zitteliana B 32 (2014) 183 bus leche: males in this group display erect posture tributing to the misplacement of Tragelaphini and when following a female during courtship (27). As Boselaphini among Antilopinae. noted above, members of the Tragelaphini, Bosela- phini and Antilopinae could have arrived at this be- Node 11 haviour through convergence. Tragelaphini + Boselaphini: these Bovinae tribes Node 6 show two informative characters; the first explains, in part, their apparently false position (separated from Hippotragini: This presents its horns high (10) Bovini) because head-and-neck-stretched-forward as opposed to the medial presentation of horns (9) posture in male courtship broadside displays (23) in other groups. Members of this tribe do not display is also present by convergence in Gazella species the head-turn in frontal dominance displays (18) nor and Alcelaphini, and two species of Caprini. The se- head-and-neck-stretched-forward posture (29) during cond character (35) corresponds to a likely Bovinae male courtship displays in following the female. The- synapomorphy with mounting with chest, chin and se two losses may be adaptations to the large size of in some instances also throat on the female’s back. the horns in these species (Lundrigan 1996). Node 12 Node 7 Caprini (united with parts of Reduncini in the tree, This group contains Tragelaphini, Boselaphini, see Fig. 2): this tribe appears monophyletic with and all Antilopinae tribes except Alcelaphini and two synapomorphies. Rising on hindlegs in hostile Hippotragini, and Kobus leche. The only informative encounters (4) is also expressed by several other character is the loss of dropping down onto knees species (Nanger granti, Aepyceros melampus, Bose- (5), present in Hippotragini and Alcelaphini and in laphus tragocamelus, Damaliscus lunatus). An evo- isolated species from other groups (Bos taurus and lutionary explanation could be a functional link bet- Boselaphus tragocamelus for Bovinae and Kobus ween the morphology of horns and the techniques leche for Antilopinae). This character seems to be of ritualized sparring displays in all Caprini species synapomorphic for each clade if the true topology (Lundrigan 1996). The loss of low presentation of follows other behavioural, morphological (Vrba & horns (11) is convergent with Bison bison, and seve- Schaller 2000) and molecular analyses (Hassanin et ral Antilopinae species. al. 2012).

Node 8 5. Conclusions

Cephalophini + Antilopini 1 (Gazella): These tribes This tentative behavioural phylogenetic analysis show two losses: erect posture in dominance fron- of bovids should be considered with caution. It is tal displays (19) and mounting with chest on the a preliminary work, relying on data obtained by re- female’s back, neck erected (38). viewing the literature. Little phylogenetic resolution could have been expected given the reduced data Node 9 set of 39 characters for 42 taxa, and the high rate of undocumented characters in some species. Gazella: This (notably without Nanger gran- Despite these limitations, some of the tribes and ti) appears monophyletic, and shows three informa- larger clades defined by morphological or molecu- tive characters: head-and-neck-stretched-forward lar analyses are supported in this behavioural ana- posture in male broadside courtship displays (23), lysis. But numerous points of discrepancy do exist lifted-head posture in following the female (28), and between this behaviour-based phylogeny and mor- mounting in standing or walking behind the female, phology- or molecular-based phylogenies. Among chest not touching the female’s back (39). Characters the unusual placements, the scattering of the ge- 23 and 28 seem to be convergent with Tragelaphini, nus Kobus is partly explainable by the high rate of Boselaphini and Bovini. Character 39 is interesting undocumented characters in these species. The because it is also present in other Antilopini species: splitting of Bovinae is due to some highly homopla- Antilope, Madoqua, Litocranius and Raphicerus, so stic and plesiomorphic characters, but it must be it could be a synapomorphy for the entire tribe. noted that character 35 “mounting with chest, chin and sometimes also throat on the female’s back” is Node 10 exclusive-ly shared by Bovini, Tragelaphini and Bo- selaphini. Given the diversity of mounting postures, This group contains Tragelaphini, Boselaphini + this char-acter could be considered as a particularly Antilopini 2 + Oreotragini + Reduncini + Caprini and reliable one, constituting a non-ambiguous synapo- is characterized by three characters (6, 16, 20) gene- morphy of Bovinae if mapped on both the molecular rally presenting a high level of homoplasy, and con- and morphological phylogenies of Fig. 1. The genus Zitteliana B 32 (2014) 184 Gazella is supported in our analysis, while Nanger Cap H, Deleporte P, Joachim J, Reby D. 2008. Male vocal behavior granti is placed outside this clade, which is consen- and phylogeny in . Cladistics 24, 917-931. sual in itself, but its far distant position in our phylo- Clauss M, Rössner GE. 2014. Old world ruminant morphophysiolo- gy, life history, and fossil record: exploring key innovations of a geny represents a major departure from the morpho- diversification sequence. Annales Zoologici Fennici 51, 80-94. logical and molecular-based analyses. Here again Deleporte P. 1993. Characters, attributes, and tests of evolutionary the mounting posture “standing behind the female” scenarios. Cladistics 9, 427-432. (39) would tend to cluster Nanger granti closer to De Queiroz K, Wimberger PH. 1993. The usefulness of behavior for Gazella. This character is also present in Litocranius phylogeny estimation: levels of homoplasy in behavioral and morphological characters. Evolution 47, 46-60. walleri and Antilope cervicapra. So, concerning the Dubost G. 1971. Observations éthologiques sur le Muntjak (Mun- unusual splitting of Bovinae and Antilopini in our ana- tiacus muntjak Zimmermann, 1780 et M. reevesi Ogilby, 1839) lysis, and mixing of parts of these groups, it seems en captivité et semi-liberté. Zeitschrift für Tierpsychology 28, that giving more weight to mounting postures could 387-427. partly correct such rather obvious misplacements. Grandcolas P, Deleporte P, Desutter-Grandcolas L, Daugeron C. 2001. Phylogenetics and ecology: as many characters as Another important character in bovids seems to be possible should be included in the cladistic analysis. Cladistics the laufschlag pattern and especially 33 “kick with the 17, 104-110. foreleg in normal or slightly erected posture” (Walther Grandcolas P, Nattier R, Legendre F, Pellens R. 2011. Mapping 1974): absent in all Bovinae, present in most of Anti- extrinsic traits such as risks or modelled bioclimatic lopinae tribes except Alcelaphini, it could be a synap- niches on phylogenies: does it make sense at all? Cladistics 27, 181-185. omorphy of Antilopinae, and would effectively appear Green MJB. 1985. Aspects of the ecology of the Himalayan musk as such if mapped on the phylogenies of Fig. 1. deer. Ph.D. Thesis, Cambridge University, Cambridge, UK, Of course, given the lasting difficulty for devising 280 p. sophisticated evolutionary models for some kinds Hassanin A, Delsuc F, Ropiquet A, Hammer C, van Vuuren BJ, Mat- of behavioural characters, the best way to improve thee C, Ruiz-Garcia M, Catzeflis F, Areskoug V, Thanh Nguyen T, Couloux A. 2012. Pattern and timing of diversification of behavioural phylogenetics of ruminants remains to cetartiodactyla (Mammalia, ), as revealed by a control for the accuracy of the available data, ob- comprehensive analysis of mitochondrial . Comptes tain data missing for some species, and expand the Rendus Biologies 335, 32-50. range of studied characters and species. Sources Irwin RE. 1996. The phylogenetic content of Avian courtship display of relevant behavioural phylogenetic characters are and song evolution. In: EP Martins (Ed), Phylogenies and the comparative method in behavior. 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Phylogenetic analysis of non-stereotyped be- fort for documenting and cross-validating a common havioural sequences with a successive event-pairing method. behavioural data base could be an efficient solution Biological Journal of the Linnean Society 94, 853-867. requiring motivation and a cooperative spirit. Legendre F, D’Haese CA, Deleporte P, Pellens R, Whiting M, Schliep K, Grandcolas P. 2014. The evolution of social behaviour in Blaberid cockroaches with diverse habitats and social systems: phylogenetic analysis of behavioural sequences. Biological Acknowledgments Journal of the Linnean Society 111, 58–77. Lorenz K. 1941. Vergleichende Bewegungsstudien an Anatiden. We sincerely thank Gertrud Rössner and the co- Journal of Ornithology 89, 194-294. Lundrigan B. 1996. Morphology of horns and fighting behavior in organizers of ICRPM2013 for offering this nice oppor- the family Bovidae. Journal of Mammalogy 77, 462-475. tunity, and William J. Silvia, Frank E. 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