Proconsul heseloni distal radial and ulnar epiphyses from the Kaswanga Primate Site, Rusinga Island, Kenya

Journal of Human Evolution 80 (2015) 17e33

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Proconsul heseloni distal radial and ulnar epiphyses from the Kaswanga Primate Site, Rusinga Island, Kenya Guillaume Daver a, *, Masato Nakatsukasa b a Institut de pal
eoprimatologie et de Pal
eontologie humaine:
evolution et pal
eoenvironnements (IPHEP), UMR-CNRS 7262, Universit
e de Poitiers, 86073 Poitiers, Cedex 9, France b Laboratory of Physical Anthropology, Kyoto University, Kyoto 6068502, Japan

a r t i c l e i n f o

a b s t r a c t

Article history: Received 20 December 2012 Accepted 12 June 2014 Available online 7 January 2015

Only two distal epiphyses of a radius and ulna are consensually attributed to the holotype skeleton of Proconsul heseloni, KNM-RU 2036. Here, we describe seven adult and immature distal antebrachial (radial and ulnar) epiphyses from two other individuals of P. heseloni from the Lower Miocene deposits of the Kaswanga Primate Site (KPS), Rusinga Island, Kenya. Because KNM-RU 2036 and KNM-KPS individuals III and VIII are conspecific and penecontemporaneous, their comparison provides the opportunity i) to characterize, for the first time, the morphological variation of the distal radioulnar joint in a Miocene ape, P. heseloni, and ii) to investigate the functional and evolutionary implications. Our results show that the distal antebrachial epiphyses of KNM-KPS III and VIII correspond to stages of bone maturation that are more advanced than those of KNM-RU 2036 (larger articulations and sharper articular borders and ligament attachments that are more developed). Accordingly, functional interpretations based solely on the skeleton of KNM-RU 2036 have involved an underestimation of the forearm rotation abilities of P. heseloni. In particular, the KPS fossils do not exhibit the primitive morphology of distal radioulnar syndesmosis, as those of KNM-RU 2036 and most nonhominoid primates, but rather the morphology of an incipient diarthrosis (as in extant lorisines and hominoids). The distal radioulnar diarthrosis permits more mobility and maintenance of the wrist during repeated and slow rotation of the forearms, which facilitates any form of quadrupedal locomotion on discontinuous and variably oriented supports. By providing the oldest evidence of a distal radioulnar joint in an early Miocene hominoid, the main conclusions of this study are consistent with the role of cautious climbing as a prerequisite step for the emergence of positional adaptations in apes. © 2014 Elsevier Ltd. All rights reserved.

Keywords: Fossil ape KPS Miocene Locomotion Forearm rotation Wrist East Africa

Introduction When compared with most other primates, living hominoids share a suite of osteological adaptations in the wrist that are related to their ability to extensively rotate their forearms (Table 1), a necessary component to be proficient in climbing and suspension. These include the presence of a distal radioulnar diarthrosis and partial or complete retreat of the ulnar styloid process from articulation with the carpus (Cartmill and Milton, 1977; Lewis, 1989; Sarmiento, 1995, 2002; Youlatos, 1996). Identification of these skeletal adaptations in the fossil record of primates, especially early Miocene catarrhines, is necessary to understand the evolutionary origin(s) of these characteristics of living hominoids.

* Corresponding author. E-mail address: [email protected] (G. Daver). http://dx.doi.org/10.1016/j.jhevol.2014.06.021 0047-2484/© 2014 Elsevier Ltd. All rights reserved.

Proconsul heseloni represents one of the best-documented hypodigms of the hominoids from the Miocene (Walker, 1997; Harrison, 2010) and is the most important reference taxon to reconstruct the positional behavior of other fossil hominoids. The postcranial skeleton of P. heseloni is currently interpreted as that of a generalized arboreal quadrupedal primate, partly engaged in some climbing activities as in colobines and large platyrrhines (Rose, 1997; Walker, 1997; Begun, 2007; Ward, 2007). Rotatory capabilities of P. heseloni forelimbs are deemed more extensive than those of the large climber platyrrhines such as Cebus, Alouatta, and Ateles, which are facilitated by a stable humeroradial joint similar to that of living hominoids (Rose, 1993, 1996). However, the morphology of its distal radioulnar joint more closely recalls the general condition seen in quadrupedal primates, including arboreal palmigrade monkeys (i.e., large platyrrhines and colobines) and terrestrial and digitigrade cercopithecines, rather than that of the more orthograde living hominoids, implying more stability of its

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Table 1 Average ranges of forearm rotation (in degrees) in descending order.a Genus Hylobates Pan Gorilla Homo Pongo Lagothrix Lagothrix Ateles Presbytis Cebus Brachyteles Alouatta Cacajao Cercopithecus Perodicticus Arctocebus Theropithecus Papio Erythrocebus Macaca

Sample size

Sample/method

Degree of rotation (standard deviation)

References

3 2 1 11 1 1 5 2 1 6 2 3 1 5 1 1 2 5 6 33

Fresh cadavers Fresh cadavers Fresh cadavers Vigil individuals Fresh cadavers Fresh cadavers Osteoligamentous preparation Fresh cadavers Fresh cadavers Fresh cadavers Skeletal remains Fresh cadavers Skeletal remains Fresh cadavers Fresh cadavers Fresh cadavers Fresh cadavers Fresh cadavers Fresh cadavers Fresh cadavers

163.0 (7.5) 160.0 160.0 156.3 (7.8) 150.0 122.0 123.3 (5.9) 122.5 120.0 118.0 (4.2) 117.5 96.7 95.0 92.0 (2.8) 90.0 90.0 90.0 (7.1) 89.0 (4.2) 87.0 (6.8) 79.0 (6.1)

O'Connor and Rarey (1979) Sarmiento (2002) Sarmiento (1988) Darcus and Salter (1953) Sarmiento (1988) Sarmiento (2002) Ziemer (1978) Sarmiento (2002) Sarmiento (2002) O'Connor and Rarey (1979) Sarmiento (2002) Sarmiento (2002) Sarmiento (2002) O'Connor and Rarey (1979) Sarmiento (1988) Sarmiento (1988) O'Connor and Rarey (1979) O'Connor and Rarey (1979) O'Connor and Rarey (1979) O'Connor and Rarey (1979)

a Standard deviation is given in brackets when documented. All measurements were taken from cadavers/skeletal samples except for humans. Data taken from skeletal remains (i.e., Brachyteles and Cacajao: Sarmiento, 2002) and those from osteoligamentous preparations (Lagothrix: Ziemer, 1978) were not distinguished.

forearm under weight-bearing conditions and a radioulnar joint as mobile as in the most arboreal and palmigrade quadrupeds (Napier and Davis, 1959; Morbeck, 1972, 1975, 1977b; Preuschoft, 1973; € n and Ziemer, 1973; Corruccini et al., 1975; O'Connor, 1976; Scho Harrison, 1982; McHenry and Corruccini, 1983; Robertson, 1984; Zylstra, 1999; Richmond and Strait, 2000). This interpretation is mainly based on numerous studies of the holotype skeleton of P. heseloni, KNM-RU 2036 (Walker et al., 1993), whose limb bones and craniodental remains were discovered in the same sedimentary block at the R114 site (Rusinga Island, Kenya) (Napier and Davis, 1959), dated at ca. 17.8 ± 0.02 Ma (millions of years ago) by both radiometric (40K/40Ar) and biostratigraphical methods (Pickford, 1986a; Drake et al., 1988). The KNM-RU 2036 skeleton was attributed to a subadult individual (female) because of unfused epiphyses of the long bones and the presence of emerging third molars (Napier and Davis, 1959; Robertson, 1984; Walker et al., 1986), but its wrist morphology is considered similar to that of an adult (Robertson, 1984; Kivell, 2007). However, the characterization of the skeletal morphology could be improved by considering individual variation with an expanded sample of specimens rather than by relying on a single individual. In the case of the distal antebrachium in Proconsul, the distal antebrachial epiphyses from KPS (Kaswanga Primate Site, site R5 on Rusinga Island) are available (Walker and Teaford, 1988; Table 2). From this site, the Joint National Museums of Kenya-Johns Hopkins University Expedition collected nine partial skeletons between

1984 and 1985, which include seven distal antebrachial epiphyses. The Proconsul skeletons from KPS and R114 were discovered 10 km away from each other in the sediments of the Fossil Bed Member, Hiwegi Formation, Rusinga Island (Beard et al., 1986, 1993; Walker and Teaford, 1988). As the antebrachial specimens of KPS were not necessarily in articulation or anatomical position, the specific and individual allocation of the KPS specimens, including sex determination, were based on their size, their state of epiphyseal union, the morphology of associated teeth and cranial remains, and their taphonomic context (Walker and Teaford, 1988; Walker et al., 1993; Begun et al., 1994). When dealing with Proconsul specimens from Rusinga (and Mfwangano), caution must be exercised with their taxonomic assignation since two Proconsul species (P. heseloni and Proconsul nyanzae) are classically recognized in this area, and the degree of morphological and metrical variation of each of them might possibly overlap (Kelley, 1986; Pickford, 1986b). However, previous researchers have provided strong evidence for supporting the close affinities (both in size and shape) between the KPS fossils and the P. heseloni holotype skeleton KNM-RU 2036. Beard et al. (1986, 1993) claimed that all of the adult carpal bones from KPS share a morphological pattern similar to that of KNM-RU 2036. Additional evidence from other mature and immature skeletal elements supports the presence of a single species at KPS, which is similar both in size and morphology to the holotype skeleton. These elements include the femora (Ruff et al., 1989), hand and foot phalanges

Table 2 Distal radial and ulnar epiphyses assigned to Proconsul included in this study.a Individuals KNM-KPS III

KNM-KPS VIII

KNM-RU 2036 a

Specimens

Anatomical part

KNM-KPS R11 (Fig. 1) KNM-KPS R12 (Fig. 1) KNM-KPS U5 (Fig. 2) KNM-KPS R5 (Fig. 1) KNM-KPS R6 (Fig. 1) KNM-KPS U2 (Fig. 2) KNM-KPS U1 (Fig. 2) KNM-RU 2036AI (Fig. 1) KNM-RU 2036AJ (Fig. 2)

Left distal radial epiphysis Right distal radial epiphysis Left distal ulnar epiphysis Right distal radial epiphysis Left distal radial epiphysis Right distal ulnar epiphysis Left distal ulnar epiphysis Left distal radial epiphysis Left distal ulnar epiphysis

Stages of bone development Adult

Locality, site, stratigraphic context Rusinga Island, KPS (R5) Hiwegi Formation, Fossil Bed Member

Subadult

Subadult

Rusinga Island, R114 Site Hiwegi Formation, Fossil Bed Member

Abbreviations: KNM, Kenyan National Museum; RU, Rusinga; KPS, Kaswanga Primate Site Table 3. Comparative sample of extant primate ulnae.

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Table 3 Comparative sample of extant primate ulnae. Taxon

Locomotor pattern/main hand posture

Specimens Wild specimens

Pan paniscus Pan troglodytes Gorilla gorilla Pongo pygmaeus Hylobatesa Symphalangus Papiob Theropithecus Macacac African colobinesd Nasalis

Semiterrestrial quadrupedalism, climbing, suspension/knuckle-walking, hook grip, palmigrady Semiterrestrial quadrupedalism, climbing, suspension/knuckle-walking, hook grip Semiterrestrial quadrupedalism, climbing/knucklewalking Arboreal: suspension and climbing/hook grip, fist walking-modified palmigrady Arboreal: brachiation and climbing/hook grip Arboreal: brachiation and more climbing than gibbons/hook grip Terrestrial quadrupedalism/digitigrady Terrestrial quadrupedalism/digitigrady Semiterrestrial quadrupedalism/palmigrady digitigrady Arboreal quadrupedalism and leaping/palmigrady Arboreal quadrupedalism, leaping and suspension/ palmigrady Arboreal quadrupedalism, climbing and suspension/palmigrady

Atelese Total a b c d e

Includes Includes Includes Includes Includes

References

Total specimens

14

14

Doran, 1989, 1993

21

31

Tuttle, 1970; Sarmiento, 1988; Doran, 1989, 1993

27

33

Tuttle, 1970; Sarmiento, 1988; Remis, 1994

12

19

18 7

27 9

Tuttle, 1967; Cant, 1987; Sarmiento, 1988; Thorpe and Crompton, 2006 Tuttle, 1972; Fleagle, 1980; Sarmiento, 1988 Tuttle, 1972; Fleagle, 1980; Sarmiento, 1988

4

23

0 7

5 26

17

23

3

5

9

11

139

226

Etter, 1973; Rose, 1977; Whitehead, 1993; Patel, 2009 Etter, 1973; Iwamoto and Dunbar, 1983; Etter, 1973; Rodman, 1979; Cant, 1988; Rawlins, 1993; Chatani, 2003 Groves, 1973; Gebo and Chapman, 1995; McGraw, 1996 Su and Jablonski, 2009 Mittermeier, 1978; Cant, 1986; Schmitt, 1994; Youlatos, 2002

the following species: H. lar (n ¼ 12); H. moloch (n ¼ 7); H. muelleri (n ¼ 3); H. concolor (n ¼ 3); H. hoolock (n ¼ 1); H. pileatus (n ¼ 1). the following species: P. anubis (n ¼ 5); P. hamadryas (n ¼ 12); P. papio (n ¼ 4); P. ursinus (n ¼ 1); P. cynocephalus (n ¼ 1). M. nemestrina (n ¼ 5), M. nigra (n ¼ 2), M. sylvanus (n ¼ 5), M. mulatta (n ¼ 8), M. sinica (n ¼ 1), M. fascicularis (n ¼ 5). C. angolensis (n ¼ 3), C. guereza (n ¼ 2), C. polykomos (n ¼ 6), Procolobus verus (n ¼ 3), P. badius (n ¼ 7), P. rufomitratus (n ¼ 2). A. paniscus (n ¼ 3), A. geoffroyi (n ¼ 8).

(Begun et al., 1994), and tibiae (Rafferty et al., 1995). All of the above-mentioned analyses corroborate Walker et al. (1993)'s conclusions that all of the KPS fossils can be attributed to P. heseloni. Even if the argument over the taxonomic attribution of the KPS Proconsul fossils has not been fully resolved, we assume that they should be assigned to P. heseloni conservatively until definitive evidence shows the presence of P. nyanzae at KPS. All of the distal radioulnar epiphyses of P. heseloni represent penecontemporaneous individuals found in a restricted and continuous geographical area. Therefore, the comparison of the epiphyses from KPS with those of R114 limits any potential biases associated with potential geographical and chronological variation. Here, we present a description of the antebrachial specimens from KPS in order to better characterize the morphological variation of the distal antebrachial epiphyses in P. heseloni and to investigate the implications, both behavioral and evolutionary. Materials and methods KPS specimens The distal antebrachial epiphyses from KPS were attributed to two female individuals of P. heseloni (Table 2; Walker and Teaford, 1988; Walker et al., 1993; Begun et al., 1994). Three specimens with complete epiphyseal union (KNM-KPS R12, right radius; KNMKPS R11, left radius; and KNM-KPS U5, left ulna) were attributed to individual III, an adult female with two nearly complete feet and a partial right hand, most of which were discovered in the topmost sediments of the locality with most bones found in anatomical position (Walker and Teaford, 1988; Begun et al., 1994). Four additional specimens, recovered from the surface, are devoid of epiphyseal union (KNM-KPS R5, right radius; KNM-KPS U2, right ulna; KNM-KPS R6, left radius; and KNM-KPS U1, left ulna) and were attributed to individual VIII, a subadult female. The body mass, based on the femoral cross section, was estimated to be

approximately 9 kg for individual III (Ruff et al., 1989), which is similar to the body mass estimated for KNM-RU 2036 (9.1e9.4 kg; Ruff et al., 1989; Ruff, 2003). Skeletal sample We compared the Proconsul distal epiphyses from KPS and R114 to their homologs in 226 extant anthropoids (Table 3). This analysis was performed at the generic level since no functional differences associated with forearm rotation abilities have been highlighted at the intrageneric level in primates (Table 1). However, we sampled only one species for each of the following apes: siamangs (Symphalangus syndactylus), orangutans (Pongo pygmaeus), chimpanzees (Pan troglodytes and Pan paniscus), and gorillas (Gorilla gorilla), in order to assess the intraspecific morphological variation seen in P. heseloni (see below for the exact randomization procedure). Only the ulnar epiphyses were compared metrically, whereas the radial parts, which were less well preserved in the KPS fossils, were only qualitatively investigated. Only individuals with emerging third molars and/or fused antebrachial epiphysis (as in KNM-RU 2036) were considered. In order to increase sample sizes, analyses were based on pooled-sex samples. The left bones were selected for measurements unless unavailable, in which case the right bone was used. Although an attempt was made to preferentially include wild-caught specimens in the comparative sample, it was not possible particularly for terrestrial (Papio, Theropithecus) and semiterrestrial monkeys (Macaca). We thus had to select specimens that were obtained from captive individuals in some instances (Table 3). The effect of captivity on morphology was investigated by Sarmiento (1985), who showed that “traits which make the hominoid wrist joint unique from that of other mammals and the orangutan wrist [and elbow] from that of other hominoids were present in captive and free-ranging orangutans” (Sarmiento, 1985:558). Thus, maximizing the sample sizes by combining wild-caught and captive individuals allows broader intertaxonomic comparisons between apes and monkeys.

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Locomotor habits and hand postures The P. heseloni antebrachial remains were compared with those of anthropoids that have varying substrate preferences (i.e., arboreal and terrestrial) and locomotor habits (i.e., quadrupedalism, climbing, and suspension). These parameters involve different degrees of forearm rotational capability (Table 3). With this aim, we collected data from highly arboreal apes that mainly use their hands as a hook during locomotion (i.e., Pongo, Hylobates, Symphalangus). Only orangutans significantly use non-stereotypical terrestrial hand postures (i.e., knuckle-walking, fist-walking, modified palmigrade postures). The other great apes are classically described as semiterrestrial and mainly knuckle-walkers even if their degree of arboreality is variable. Bonobos and chimpanzees were treated separately because bonobos use more suspension than chimpanzees (Doran, 1993) and are more palmigrade due to their extensive use of boughs and branches (Doran, 1989, 1993). Cercopithecoids include i) arboreal palmigrade monkeys, such as African colobines, and the more suspensory proboscis monkey (Nasalis), ii) terrestrial and digitigrade primates, such as baboons (Papio) and geladas (Theropithecus; here distinguished from baboons since they live in treeless habitats of the Ethiopian highlands; Iwamoto and Dunbar, 1983), and iii) semiterrestrial palmigrade/digitigrade macaques (Macaca). All macaques combine various proportions of arboreality and terrestriality as well as palmigrady and digitigrady (Tuttle, 1969a; Rawlins, 1993; Chatani, 2003). Even the most arboreal macaque species, Macaca fascicularis, uses digitigrady (Tuttle, 1969a) and has been seen moving and feeding on the ground near the banks of large streams (Cant, 1988). Spider monkeys (Ateles) were also included since they have been described as good modern analogs for understanding the € n and Ziemer, 1973; functions of the wrists in P. heseloni (Scho Youlatos, 1996). However, among atelines, only spider monkeys have been shown to be morphologically and functionally convergent with apes at their antebrachiocarpal joint (in contrast to howler monkeys; Youlatos, 1996). Methods From the relatively well-preserved ulnae of KNM-KPS VIII (KNM-KPS U2) and KNM-RU 2036 (KNM-RU 2036AJ), five measurements were taken to quantify the structure of the styloid process and ulnar head. In apes, these structures bear the osteological correlates of the distal radioulnar diarthrosis and partial or complete retreat of the ulnar styloid process from articulation with the carpus. With one exception, all of these measurements have been defined and used earlier (Table 4; Fig. 1). The more poorly preserved specimen, KNM-KPS III (KNM-KPS U5), only allowed partial measurements to be taken.

With regards to the ulnar styloid process, the proximodistal length of the styloid process (PDsp) distinguishes between the relatively reduced styloid process of extant hominoids and the longer one of extant nonhominoids (O'Connor, 1975). For comparative purposes, we also measured the maximum dorsopalmar diameter of the epiphysis (DPm), as this measurement is typically used for ratio computations of the relative length of the styloid process (Napier and Davis, 1959; Harrison, 1982; Hamrick et al., 2000; Drapeau et al., 2005). Also, the mediolateral diameter of the styloid process (MLsp) is required for distinguishing apes from monkeys since apes (as in lorisines) exhibit a styloid process described as a “relatively slender projection” (Cartmill and Milton, 1977:253), a morphology that is particularly well expressed in Hylobates and Pan, two apes that also retain a reduced ulnotriquetral contact (Sarmiento, 1988). With regards to the ulnar head, the degree of extension of the surfaces for the radius and the triangular ligament on the ulna was quantified in order to assess the degree of forearm rotation. Thus, we measured the mediolateral length (MLa) and the dorsopalmar length (DPa) of the distal articular facet on the ulnar head. Dorsopalmar length is not homologous with the measurement from Corruccini (1978), and McHenry and Corruccini (1983). These authors measured the length between the most distal projection of the distal articular surface and its dorsal border. However, the radial facet on the ulnar head, although continuous with the distally directed articular surface, is laterally oriented (O'Connor, 1975). For this reason, we chose to measure the DPa from the most palmar projection of the distal ulnar surface to its most dorsal projection. Additionally, we do not take the maximum mediolateral diameter of the ulnar head (as in Corruccini et al., 1975; Harrison, 1982; Hamrick et al., 2000; Drapeau et al., 2005) because this measurement is not homologous between apes and monkeys. Indeed, the maximum diameter of the ulnar head is similar to the MLa in apes, whereas the maximum diameter of the ulnar head includes a dorsal tubercle in monkeys, which is not relevant for estimating the abilities of forearm rotation. Measurements were taken from digital photographs using ImageJ software (Abramoff et al., 2004). The digital camera was placed with its lens perpendicular to the object at a distance of at least 12 times the object's size to reduce parallax (Spencer and Spencer, 1995; Patel, 2005). A scale was photographed simultaneously to calibrate the photographs. Photographs were taken of the distal and palmar views. The measurements were taken to the nearest tenth of a millimeter. From the linear measurements, three indices were calculated to quantify i) the length of the styloid process relative to the dorsopalmar diameter of the ulnar head (PDsp/DPm), ii) the robustness of the styloid process (MLsp/PDsp), and iii) the relative breadth of the distal articular surface for the triangular ligament (MLa/DPa).

Table 4 Ulnar epiphyses measurements. Measurements MLa: mediolateral length of the distal radial facet on the ulnar head DPm: maximum dorsopalmar diameter of the ulnar epiphysis DPa: dorsopalmar length of the distal articular facet on the ulnar head PDsp: proximodistal length of the ulnar styloid process MLsp: mediolateral diameter of the styloid process

Definition From distal view, taken from the most medial extent to the most lateral extent of the ulnar head articular surface (as in Corruccini et al., 1975; Ciochon, 1986; Drapeau et al., 2005) From distal view, measured from the most palmar projection of the ulnar head articular surface to the most dorsal projection of the styloid process (as in Napier and Davis, 1959; Corruccini et al., 1975; Ciochon, 1986; Harrison, 1982; Drapeau et al., 2005) From distal view, taken from the most palmar projection of the distal articular surface to its most dorsal projection, perpendicular to the long mediolateral axis of the surface From palmar view, measured as the proximodistal length of the ulnar styloid process over the most distal part of the radial facet of the ulna (as in Corruccini et al., 1975; Corruccini, 1978; Harrison, 1982; McHenry and Corruccini, 1983; Ciochon, 1986; Inouye, 1991) From palmar view, taken from the most dorsomedial projection of the ulnar styloid process to its most lateralpalmar projection (as in Ciochon, 1986; Hamrick et al., 2000)

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Figure 1. Measurements used in this study as illustrated on distal ulnae of a chimpanzee (Pan troglodytes; left) and a pig-tailed macaque (Macaca nemestrina; right) in palmar (upper) and distal (bottom) views. Measurements taken are as follows; MLa: mediolateral length of the distal radial facet on the ulnar head; DPm: maximum dorsopalmar diameter of the ulnar epiphysis; DPa: dorsopalmar length of the distal radial facet on the ulnar head; PDsp: proximodistal length of the ulnar styloid process; MLsp: mediolateral diameter of the styloid process. Measurements are defined in Table 4 and discussed in the text. Scale bar, 10 mm.

Finally, principal component analysis (PCA) and canonical variate analysis (CVA) were performed on the size-adjusted measurements of the distal ulna. The PCA aims to explore the interindividual variation by maximizing the variance between individuals, whereas the CVA is designed to test the discrimination between taxonomic units by maximizing the intergroup variance. For these multivariate analyses, the shape variables were calculated from the five raw measurements, following the methods of log-shape ratios (Mosimann, 1970; DeSilva et al., 2010). The log-shape ratios (shape variable) were calculated with the formula log(Xi/G), where G, the geometric mean (or size variable), was calculated as the nth root of the product of n raw measurements, and Xi is a raw measurement. Because CVAs are proven to be sensitive to unbalanced samples (as in this study; Mitteroecker and Bookstein, 2011), an effort was made to use a number of individuals per sample at least equal to the number of variables (n ¼ 5). The results were analyzed in PAST (Hammer et al., 2001). The significance of differences between group means was assessed by using a permutation test: a post hoc analysis (Hotelling's T2 test) allows testing the significance of the equality of means between two groups of the sample by permutation. The significance of differences between groups is illustrated by a probability p to reject the null hypothesis ‘means of two groups are equal' is inferior to 0.05. The pairwise comparisons use the within-group covariance matrix pooled over all groups participating in the MANOVA. Given the variation in shape identified between the fossil ulnae (differences in size being less notable), and that the two fossil ulnae are supposedly from two subadult females, we assessed the likelihood of observing two extant specimens with a shape difference at least equal to the difference seen between the two P. heseloni ulnae. To do that, we used an exact randomization procedure applied to the size-adjusted variables (Richmond and Jungers, 1995; Aiello et al., 1999). We calculated the shape differences between the five size-adjusted ulnar measurements (¼ overall shape difference between two specimens) between all possible pairs of specimens from each taxonomic group. Shape differences, independent of size, are based on the size-corrected average

taxonomic distance (Richmond and Jungers, 1995; Aiello et al., 1999). This is computed as follows:

vffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi !2ffi u u X1 x xkj t ki Eij ¼  n GMi GMj k

where: Eij: average distance between individuals i and j P k: sum of values for the character k n: number of measurements used for a specimen GMi and GMj: respective geometric means of specimens i and j xki: value of the character k for the specimen i xkj: value of the character k for the specimen j After this computational step, the proportion of distances in a taxon that are greater or equal to the distance between the two fossil ulnae provides the likelihood (expressed in %) of sampling two individuals as different in shape as the fossils. Results Descriptions of the KPS distal radial epiphyses (Fig. 2) Preservation The left radius of KNM-KPS VIII (KNM-KPS R6) is the most informative specimen among the KPS radii. This specimen preserves the palmar surface of the styloid process, the scaphoid facet, the dorsopalmarly widest portion of the lunate facet, and the apex of the dorsal tubercle. Unfortunately, the specimen is severely eroded along its metaphyseal line and along the palmar and medial borders of the lunate facet and lacks the entire dorsal surface. The right radius of the same individual (KNM-KPS R5) is more severely damaged and adds no additional information. With regard to the other individual (KNM-KPS III), the left radius (KNM-KPS R11) is better preserved than the right specimen (KNM-KPS R12). KNMKPS R11 preserves the palmar surface of the styloid process, the

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scaphoid facet, and the distal apex of the dorsal tubercle. However, the lunate facet and the dorsal surface of the epiphysis are crushed due to postdepositional dorsopalmar compression. Additionally, the lunate facet is largely eroded along its palmar and medial borders. In the right counterpart (KNM-KPS R12), the entire palmar surface is crushed and distorted. However, only this specimen preserves the dorsal surface, including the dorsal aspect of the styloid process and the dorsal tubercle. Unfortunately, no specimens preserve the ulnar notch, and the preservation of the lunate face is poor. Thus, unlike previous studies (e.g., Corruccini, et al., 1975; Corruccini, 1978; McHenry and Corruccini, 1983; Zylstra, 1999; Richmond and Strait, 2000; Corruccini and McHenry, 2001), a metric analysis of the radial styloid process projection and the proportions and orientations of the carpal facets are not possible in this study. However, several qualitative features (e.g., the overall morphologies of the carpal facets and the areas of the attachments of ligaments and muscles)

allow the morphological affinities and functional interpretations of the fossil radii to be characterized. Comparative morphology and functional interpretations The radii of KNM-KPS III, VIII, and KNM-RU 2036AI show no substantial morphological differences from each other with regard to the overall size and shape of the carpal articular surfaces and the attachment areas of muscles and ligaments (Fig. 2). The carpal facets in KNM-KPS VIII (KNM-KPS R6) are at a high angle (approximately 160 ), which causes these two carpal facets to be almost coplanar, similar to those of KNM-RU 2036 and extant quadrupedal monkeys (i.e., knuckle walker, digitigrade, semidigitigrade, and palmigrade primates; trait labelled 1 on Fig. 2; Jenkins and Fleagle, 1975; Richmond and Strait, 2000). In these primates, the coplanarity of the carpal facets presumably aids in resisting stresses in the radioulnar plane (Jenkins and Fleagle, 1975). In suspensory Asian apes, the carpal facets are at a lower angle in relation to each other, which might contribute to a ball-

Figure 2. Distal radial epiphyses from KPS and R114. Top row, from left to right: palmar views in an orangutan (Pongo), a proboscis monkey (Nasalis), two langurs (Semnopithecus and Trachypithecus), and an owl monkey (Aotus). Middle row, from left to right: dorsal view of KNM-KPS R12 (left radius); mediopalmar view of KNM-KPS R5 (right radius); palmar views of KNM-KPS R11 (left radius); and KNM-KPS R6 (left radius); palmar and dorsal view of KNM-RU 2036AI (left radius). Bottom row, from left to right: distal view of KNM-KPS R5; KNM-KPS R11; KNM-KPS R6; and KNM-RU 2036AI. Numbers 1 to 4 denote characters explained in Table 6: 1, the coplanarity of radiocarpal facets; 2, a rounded lunate facet, which is dorsopalmarly extensive relatively to the scaphoid facet; 3, a flat and large dorsal tubercle lying dorsal to the lunate facet; 4, a deep and extensive attachment area for a bifascicular radiocarpal ligament on the styloid process. Comparison with extant primates (specimens of Pongo and Trachypithecus come from individuals with emerging third molars) shows that P. heseloni is closer to suspensory apes with regards to character 4. The three specimens of Semnopithecus, Trachypithecus, and Aotus were not included in the quantitative analysis since the ulnae were not available for study. Scale bar, 10 mm.

G. Daver, M. Nakatsukasa / Journal of Human Evolution 80 (2015) 17e33

and-socket mechanism (Corruccini et al., 1975; Jenkins and Fleagle, 1975; Richmond and Strait, 2000). The overall shape of the scaphoid facets is roughly similar in the specimens from KPS and R114. As in KNM-RU 2036, the lunate facet in KNM-KPS VIII (KNM-KPS R6; not preserved in KNM-KPS III) has rounded contours. Interestingly, the radius of KNM-RU 2036 exhibits smooth articular borders and the smallest carpal facets among the P. heseloni radial specimens, which could be due to this individual being at an earlier stage of development. Despite these later differences, all of the P. heseloni specimens, similar to extant monkeys, display a rounded lunate facet (labelled 2 in Fig. 2). This morphology is functionally associated with an emphasis on the €n weight support functions of the ulna (Morbeck, 1972, 1975; Scho and Ziemer, 1973; Corruccini et al., 1975; Jenkins and Fleagle, 1975; O'Connor, 1975; McHenry and Corruccini, 1983; Sarmiento, 1988; Zylstra, 1999; Richmond and Strait, 2000). In extant apes, reduction of ulnar-side weight support is exemplified by a narrow radial articular area of lunate relative to the radial articular area of the scaphoid (Sarmiento, 1987). In all specimens from KPS, the distal apex of the dorsal tubercle lies dorsal to the lunate facet (labelled 3 in Fig. 2). The tubercle is broad mediolaterally and flat dorsally. The adult individual KNMKPS III (KNM-KPS R12) differs slightly from the other Proconsul individuals in exhibiting a dorsal tubercle with an accentuated relief, which may represent the mature state of this trait in this taxon. The overall morphology observed on the KPS radii is similar to that found in KNM-RU 2036AI and extant cercopithecoids (O'Connor, 1976). In extant apes, the dorsal radial tubercle is narrow mediolaterally and rounded dorsally and lies dorsal to the scaphoid facet on the distal radius (O'Connor, 1975). The dorsal tubercle delineates the grooves for the tendons of the extensor muscles (medially, m. extensor digitorum; laterally, mm. extensor carpi radialis brevis and longus). In macaques, these muscles engage in extending, abducting (particularly mm. extensor carpi radialis brevis and longus), and flexing (particularly m. extensor carpi radialis brevis) the hands during quadrupedal walking; these muscles can also function as synergists with the flexor muscles (Kikuchi, 2004). Therefore, a dorsally flat and mediolaterally broad dorsal tubercle provides a firm anchorage for the extensor retinaculum and for better maintenance of the tendons of the extensor muscles. This morphology in P. heseloni serves to improve the stabilization of the hands during quadrupedal walking. The palmar surface of the styloid process of the KPS radii bears a deep and extensive indentation for the attachment of a bifascicular

23

radiocarpal ligament similar to those found in KNM-RU 2036AI and extant hominoids (Lewis, 1972, 1989). However, this indentation is more pronounced on the KPS specimens than on KNM-RU 2036AI, which likely represents the mature state of this trait in P. heseloni (labelled 4 on Fig. 2). Although an indentation for the bifascicular radiocarpal ligament is also observed in extant non-hominoid anthropoids (Morbeck, 1975; Sarmiento, 1985), it is never as extensively developed as in hominoids (Sarmiento, 1985). A bifascicular radiocarpal ligament provides better stability of the wrist during supination, extension, and ulnar deviation (Ziemer, 1978; Kapandji, 2005). However, the pronounced development of this ligament in apes shows that it provides stability in supination during their frequent forearm rotation, which is advantageous for their antipronograde behaviors such as suspension (Lewis, 1971, 1972) and cautious climbing (Sarmiento, 1985, 1987, 1988). If this interpretation is correct, the radially stabilized wrist of P. heseloni might also facilitate such antipronograde behaviors. Descriptions of the KPS distal ulnar epiphyses (Fig. 3) Preservation The epiphysis of the right ulna in KNM-KPS VIII (KNMKPS U2) is the best-preserved specimen among the KPS ulnae, which is complete except for the slight erosion of the cortical surface and slight erosion along the metaphyseal surface. The left counterpart (KNM-KPS U1) suffers from general surface erosion and lacks the dorsomedial portion of the styloid process as well as most part of its metaphyseal portion. Nonetheless, this specimen preserves the palmar portion of the ulnar head as well as the entire lateropalmar portion of the styloid process. The left ulna of KNMKPS III (KNM-KPS U5) is the least-preserved specimen, missing the palmar portion of the ulnar head and the styloid process. This specimen has been compressed dorsopalmarly, which has introduced cracks at the medial base of the styloid process. However, the ulnar fovea is clearly visible as is most of the distal surface for the triangular ligament. Comparative morphology and functional interpretations The ulnae of KNM-KPS III and VIII show no substantial differences regarding their overall size and, although at a lesser degree, their shape (Table 5). KNM-KPS U1 and U2 are similar in size to that of KNM-RU 2036AJ. The styloid process of KNM-KPS VIII projects distally as much as that of KNM-RU 2036 (labelled 5 in Fig. 3). These processes resemble those of gibbons (Hylobates) and do not exceed the variation seen in monkeys (Table 5; Fig. 4). For this feature, P. heseloni

Table 5 Distal ulnar epiphyses measurements (mm).a Taxon/specimen

Sample size

MLa

DPm

DPa

KNM-RU 2036AJ KNM-KPS U5 KNM-KPS U2 KNM-KPS U1 Pan paniscus Pan troglodytes Gorilla Pongo Symphalangus Hylobates Papio Theropithecus Macaca African colobines Nasalis Ateles

1 1 1 1 14 31 33 19 9 27 23 5 26 23 5 11

6.7 >8.5 9.2 e 18.1 ± 1.2 19.7 ± 1.6 26.4 ± 4.1 22.9 ± 3.2 11.7 ± 1.4 8.9 ± 0.8 7.8 ± 1.7 6.3 ± 1.0 6.4 ± 1.3 6.0 ± 1.0 8.8 ± 1.2 5.5 ± 0.8

11.4 e 11.8 12.3 20.0 ± 0.6 21.7 ± 1.8 28.9 ± 4.2 23.5 ± 2.6 13.5 ± 1.0 11.4 ± 0.8 14.3 ± 2.1 12.1 ± 0.6 11.0 ± 1.6 10.9 ± 1.1 14.1 ± 1.2 9.6 ± 1.0

3.7 >3.7 3.2 e 6.3 ± 0.7 6.4 ± 1.1 10.2 ± 1.8 8.2 ± 1.6 3.4 ± 0.8 3.1 ± 0.4 4.2 ± 1.5 3.4 ± 0.6 3.3 ± 1.1 3.2 ± 0.9 5.1 ± 0.9 2.4 ± 0.7

PDsp 6.2 e 6.1 6.7 2.6 5.1 1.8 3.4 4.8 5.0 6.5 6.1 5.2 4.2 6.0 5.1

± ± ± ± ± ± ± ± ± ± ± ±

0.9 1.6 1.7 2.1 1.0 1.0 1.1 0.8 0.9 0.7 0.6 0.7

MLsp 5.3 e 5.9 3.9 5.9 7.0 5.3 6.7 4.0 3.6 6.6 5.1 4.9 5.3 6.6 5.4

± ± ± ± ± ± ± ± ± ± ± ±

1.2 1.0 3.9 3.5 0.7 0.5 0.7 0.7 0.7 0.7 0.8 0.5

a All measurements are reported as the means ± 1 standard deviation. MLa, mediolateral length of the distal radial facet on the ulnar head; DPa, dorsopalmar length of the distal articular facet on the ulnar head, PDsp, proximodistal length of the ulnar styloid process; MLsp, mediolateral diameter of the styloid process; DPm, maximum dorsopalmar diameter of the ulnar head.

24

G. Daver, M. Nakatsukasa / Journal of Human Evolution 80 (2015) 17e33

Figure 3. Distal ulnar epiphyses from KPS and the R114 site. Top row, from left to right: medial views of KNM-KPS U2 (right ulna), KNM-KPS U5 (left ulna), KNM-KPS U1 (left ulna), and KNM-RU 2036AJ (left ulna) and of an ulna from a proboscis monkey (Nasalis). Middle row, from left to right: distal views of KNM-KPS U2 (right ulna), KNM-KPS U5 (left ulna), KNM-KPS U1, and KNM-RU 2036AJ. Bottom row, from left to right: distal views of ulnae of an orang-utan (Pongo), a gibbon (Hylobates), a spider monkey (Ateles), a proboscis monkey (Nasalis), and a macaque (Macaca). Numbers 5 to 8 denote characters explained in Table 6: 5, a long styloid process that contacts the carpus; 6, an enlarged distal surface for the triangular ligament; 7, a kidney-shaped distal surface for the triangular ligament, and 8, deep ulnar fovea for the attachment of the ulnocarpal ligaments. Comparison with extant primates (all specimens come from individuals with emerging third molars) shows that P. heseloni is closer to suspensory apes with regards to the characters 6, 7 and 8. Scale bar, 10 mm.

differs from the great apes (i.e., Pan, Gorilla, Pongo) and siamangs (Symphalangus), which are characterized by a relatively shorter styloid process. In addition, KNM-KPS VIII and KNM-RU 2036 have a relatively slender styloid process (Table 5; Fig. 5) similar to many other primates, including Pan troglodytes, Hylobates, Symphalangus, and all monkeys. This generalized condition substantially differs from the more robust styloid process that is found in Pan paniscus, Gorilla, and Pongo. This result confirms the previous comparisons of KNM-RU 2036AJ that have highlighted the monkey-like aspect of the styloid process in P. heseloni (Napier and Davis, 1959; Morbeck, € n and Ziemer, 1973; O'Connor, 1976; Harrison, 1972, 1977a; Scho 1982; Robertson, 1984; Beard et al., 1986; Sarmiento, 1988). The function of a long styloid process that contacts the carpus is to stabilize the ulnocarpal joint under weight-bearing conditions (Lewis, 1965, 1989; Conroy and Fleagle, 1972; O'Connor, 1975; Cartmill and Milton, 1977; Mendel, 1979; Sarmiento, 1987, 1988) and to limit the radioulnar deviation of the proximal carpal row as in digitigrade, semidigitigrade, and palmigrade monkeys (O'Connor, 1975; Jouffroy and Medina, 2002; Daver et al., 2012). The articular surface for the triquetrum and the pisiform is eroded in

KNM-KPS U2 and KNM-KPS U1 (Fig. 3). However, the associated triquetrum and pisiform of both individual III and VIII show clear articular surfaces for the styloid process as in KNM-RU 2036 (Beard et al., 1986, 1993). Two features of the KPS ulnae (KNM-KPS U2 and KNM-KPS U5) differ from those of KNM-RU 2036AJ. The differences are especially marked in KNM-KPS U5, which suggests that these differences are related to the immaturity of KNM-RU 2036. First, the shape of the distal articular surface in the KPS individuals is characterized by an enlarged and kidney-shaped distal surface for the triangular ligament (Fig. 6; labelled 6 and 7 in Fig. 3). This condition differs from that of KNM-RU 2036AJ, digitigrade and semidigitigrade monkeys (i.e., baboons and macaques), and palmigrade monkeys (i.e., colobines and atelines), which have a distal surface that is mediolaterally narrow with ovoid contours. Among extant primates, only apes and lorisines are characterized by a kidney-shaped distal articular surface of the ulna (Sarmiento, 1987, 1988; Hamrick et al., 2000). Such morphology is classically associated with an extensive ability for forearm rotation (ranging between 150 and 163 ; Sarmiento, 2002). Interestingly, the adult

G. Daver, M. Nakatsukasa / Journal of Human Evolution 80 (2015) 17e33

25

KNM−KPS U2

KNM−KPS U2 KNM−RU 2036AJ Ateles Nasalis African colobines Macaca Theropithecus Papio Symphalangus Hylobates Pongo Gorilla Pan troglodytes Pan paniscus

KNM−RU 2036AJ Ateles Nasalis African colobines Macaca Theropithecus Papio Symphalangus Hylobates Pongo Gorilla Pan troglodytes Pan paniscus

0.0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

PDsp/DPm

individual KNM-KPS III (KNM-KPS U5) differs from KNM-RU 2036 (KNM-RU 2036AJ) and KNM-KPS VIII (KNM-KPS U2) by having a distal articular facet with a sharper dorsal edge (i.e., not smooth like those of KNM-RU 2036AJ and KNM-KPS U2). Second, the ulnar fovea (the space located between the styloid process and the articular surface for the triangular ligament) on KPS individuals (KNM-KPS U2 and U5) bears a deep fossa for the attachment of the triangular ligament and ulnocarpal ligaments (labelled 8 on Fig. 3) as in apes, a condition absent in KNM-RU 2036AJ and extant platyrrhine and cercopithecoid monkeys (Napier and Davis, 1959; Corruccini et al., 1975; Corruccini, 1978; Harrison, 1982; McHenry and Corruccini, 1983; Sarmiento, 1985) (see Figure 2 for an illustration of this feature, see Fig. 3 where distal views of cercopithecoid and ateline ulnae are shown as well as a medial view of the ulna in Nasalis). Extant apes are characterized by a deep fossa on the ulnar fovea that suggests the presence of a triangular ligament and strong ulnocarpal ligaments (Lewis, 1965,

KNM−KPS U2 KNM−RU 2036AJ Ateles Nasalis African colobines Macaca Theropithecus Papio Symphalangus Hylobates Pongo Gorilla Pan troglodytes Pan paniscus 0.7

0.8

0.9

0.4

0.6

0.8

1.0

MLa/DPa

Figure 4. Length of the styloid process relative to maximum diameter of the ulnar head (PDsp/DPm) in two individuals of P. heseloni, KNM-KPS VIII (KNM-KPS U2) and KNM-RU 2036 (KNM RU 2036AJ), compared with extant anthropoids. The box represents the 25th and 75th percentiles, the center line is the median, the whiskers represent the non-outlier range, and the dots are outliers.

0.6

0.2

1.0

1.1

MLsp/PDsp Figure 5. Robustness of the styloid process (MLsp/PDsp) in two individuals of P. heseloni, KNM-KPS VIII (KNM-KPS U2) and KNM-RU 2036 (KNM RU 2036AJ), compared with extant anthropoids. For symbols, see Figure 4.

Figure 6. Morphology of the distal ulnar surface (MLa/DPa) in two ulnae of P. heseloni, KNM-KPS VIII (KNM-KPS U2) and KNM-RU 2036 (KNM RU 2036AJ), compared with extant anthropoids. For symbols, see Figure 4.

1971, 1972; Sarmiento, 1987, 1988). In extant hominoids, the ulnar long axis experiences repeated oscillations around the radial long axis during forearm rotation. In this context, the presence of a triangular ligament and strong ulnocarpal ligaments help in maintaining the ulnar epiphysis against the radial epiphysis while allowing more mobility of the distal radioulnar joint (Sarmiento, 1988; Jouffroy and Medina, 2002). This function was most likely enhanced in P. heseloni. Multivariate analyses The one aspect of the KPS specimens that can be meaningfully compared quantitatively across samples is the general ulnar morphology. For a multivariate analysis, only the study of KNM-KPS U2 allows for adequate quantified comparisons with KNM-RU 2036AJ. As noted earlier, principal components analysis (PCA) and canonical variate analysis (CVA) were used to explore the interindividual and intertaxonomic variation of the ulnar morphology in anthropoids including the P. heseloni ulnae (KNM-KPS U2 and KNM-RU 2036AJ). With regards to the PCA (Fig. 7; Table 7), the projection plane is composed of the two first principal axes, which summarize more than 93% of the total variance. This plane separates great apes (on the left) from monkeys (on the right), with gibbons and siamangs being intermediate. The differentiation between these three groups is mainly influenced by the variation of i) the length of the styloid process (PDsp; on PC1), ii) the mediolateral length of the distal ulnar facet (MLa; PC1 and PC2), and iii) the mediolateral lengths of the styloid process (PC2; Table 7). The first PC (85.2% of total variance) separates great apes from monkeys, and gibbons and siamangs are intermediate. KNM-KPS U2 and KNM-RU 2036AJ do not seem to exceed the variation seen in most monkeys (i.e., Papio, Macaca, Nasalis, and Ateles). Although KNM-RU 2036AJ appears strictly monkey-like, KNM-KPS U2 shows morphological affinities closer to gibbons. The present PCA also underlines the strong influence of the morphological variation of the styloid process of anthropoids in multivariate analyses. This result is illustrated by the large disparity of the specimens along the first axis of the PCA, which confirms the results from previous multivariate comparisons of the KNM-RU 2036 ulna (Zwell and Conroy, 1973; Corruccini et al., 1975; McHenry and Corruccini, 1983).

26

G. Daver, M. Nakatsukasa / Journal of Human Evolution 80 (2015) 17e33

Pan paniscus Pan troglodytes Gorilla Pongo Hylobates Symphalangus African colobines Papio Macaca Ateles Theropithecus Nasalis Proconsul heseloni

Principal component 2 (7.86% of variance)

2.4 1.8 1.2

KNM-RU 2036AJ

0.6 0

KNM-KPS U2

-0.6 -1.2 -1.8 -2.4 -3

-3.6

-3

-2.4 -1.8 -1.2 -0.6 0 Principal component 1 (85.52% of v ariance)

0.6

1.2

Figure 7. Principal components analysis of the distal ulnar epiphyses of P. heseloni and extant anthropoids.

We also performed a CVA (Fig. 8; Table 8 to assess the intertaxonomic variation of the P. heseloni ulnae compared with other anthropoids. The two first canonical axes summarize more than 95% of the total variance. The post-hoc Hotelling's pairwise comparisons show that extant monkeys are significantly discriminated from apes (p << 0.05; Table 9). As far as the fossils are concerned, P. heseloni is not distinguishable from hylobatids and monkeys. Overall, the analysis highlights the distinct morphological affinities of each P. heseloni ulnae. KNM-RU 2036AJ remains typically

monkey-like, whereas KNM-KPS U2 does not exceed the variation of gibbons as an outlier. Therefore, the hypothesis that the distal ulnar end of P. heseloni may have been similar to that of modern monkeys exclusively is not supported by this analysis. The procedure of exact randomization was applied to all species of extant apes (except for Symphalangus) and for the largest sample of monkeys in our extant sample (i.e., Macaca and Papio). This exact randomization shows that all of the extant taxa exhibit variations of shape at least as great as that seen between the two fossils

Table 6 Morphology of Proconsul heseloni compared with that of extant hominoids.a

Radial characters

Ulnar characters

Definitions of characters

Associated functions

Morphology in extant hominoids compared with other primates

Morphology in Proconsul heseloni

Angulation of scaphoid and lunate facets

Resist to compressive forces in the radioulnar plane

Absent (coplanar; Fig. 1)

Narrow lunate facet on the radius compared to the scaphoid facet Radial dorsal tubercle lying dorsally to the scaphoid facet Deep and extensive attachment fossa for the bifascicular palmar developed ligament Nonarticulating ulnar styloid process (which suggests the presence of the semilunar meniscus)

De-emphasis on ulna for weight support functions Infrequent use of hyperextended hand posture Mainly stability of supination (to a lesser extent, extension and ulnar deviation) Stability for forearm rotation and the resulting oscillations of the ulnar styloid process

Present in Asian hominoids in contrast to other anthropoids (1, 5, 17) Present in contrast to other primates (5, 13, 15, 17) Present in contrast to other primates (13) Present in contrast to other anthropoids (6, 15)

Rounded morphology of the ulnar head due to an enlarged distal articular surface Extended contact with triangular ligament suggested by a kidneyshaped distal articular surface on ulnar head Presence of strong ulnocarpal ligaments suggested by a deep ulnar fovea

Mobility for forearm rotation

Mobility for forearm rotation

Stability of forearm rotation

Present in hominoids in contrast to other primates (presence of articular surface for the meniscus in Pan and Hylobates; 1, 4, 6, 7, 8, 9, 10, 11, 12, 14, 15, 18) Present in contrast to other primates (except lorisines; 3, 4, 6, 7, 8, 9, 13, 15) Present in contrast to other primates (3, 4, 6, 7, 8, 9, 13, 15)

Present in contrast to other primates (2, 11, 12, 16)

Absent (Fig. 2) Absent (Fig. 2) Present (Fig. 2)

Absent (Fig. 3)

Present (Fig. 3)

Present (Fig. 3)

Present (Fig. 3)

a In bold, characters shared by P. heseloni and extant hominoids. Sources of the morphological traits listed in Table: 1, Corruccini et al. (1975); 2, Corruccini (1978); 3, Cartmill and Milton (1977); 4; Harrison (1982); 5, Jenkins and Fleagle (1975); 6, Lewis (1989); 7, Lewis (1965); 8, Morbeck (1975); 9, Morbeck (1972); 10, Morbeck (1977a); 11, McHenry and Corruccini (1983); 12, Napier and Davis (1959); 13, O'Connor (1975); 14, Robertson (1984); 15, Sarmiento (1988); 16, Sarmiento (1987); 17, Richmond and Strait €n and Ziemer (1973). (2000); 18, Scho

G. Daver, M. Nakatsukasa / Journal of Human Evolution 80 (2015) 17e33 Table 7 Results of the principal components analysis: eigenvalues and percentages of total variance and loadings.a

Eigenvalue %variance MLa DPa PDsp MLsp DPm a

PC 1

PC 2

PC 3

0.595132 85.516 ¡0.3794 0.2778 0.8469 0.2002 0.1467

0.054674 7.8562 ¡0.6027 0.4358 0.2739 0.6096 0.01528

0.0372887 5.3581 0.1834 0.7368 0.2859 ¡0.5812 0.06318

Table 8 Results of the canonical variate analysis: eigenvalues and percentages of total variance and loadings.a

Eigenvalue %variance MLa DPa PDsp MLsp DPm a

The two highest loadings are shown in bold.

(although in variable proportions). The value of the size-corrected average taxonomic distance between the fossils is 0.152 and the probabilities to find a difference as great as this value in the extant taxa are as follows: P. paniscus, 40.7%; P. troglodytes, 46.4%; Gorilla gorilla, 73%; P. pygmaeus, 69.6%; Hylobates, 33.1%, Macaca, 48.6%; Papio, 57.7%. As a result, this study cannot reject the hypothesis that the KNM-KPS U2 and KNM-RU 2036 belong to the same species (i.e., P. heseloni) on the criteria of shape variations. Discussion Although the varying states of preservation of the P. heseloni distal antebrachial epiphyses from KPS preclude statistically rigorous morphological analyses, this study highlights the substantial individual variation that secondarily allows reassessment of the functions of the distal radioulnar joint for P. heseloni as well as their behavioral and evolutionary implications. Interpretation of the individual variation The antebrachii from KPS differ from those of KNM-RU 2036 by i) larger articular surfaces (radiocarpal facets and distal ulnar facet), ii) articular borders that are sharper (distal articular surface of the ulna, KNM-KPS U5), and iii) reliefs for ligament attachments that are more accentuated (deep and extended attachments for the palmar radiocarpal ligament, deep fossa for the ulnocarpal

CV 1

CV 2

8.725 77.94 ¡0.10741 0,048901 0.018537 0.058002 0.02788

1.954 17.45 0.004478 0.071906 ¡0.019218 0.052648 0.034594

The two highest loadings are shown in bold.

ligaments and triangular ligaments). Additionally, the distal antebrachium of KNM-KPS III exhibits some slight variations compared with those of KNM-RU 2036 and KNM-KPS VIII (i.e., an accentuated dorsal tubercle for the sheath of the extensor muscles and sharper contours of the articular surface for the triangular ligament in the distal antebrachium of KNM-KPS III). Such morphological variations are typically associated with different stages of bone maturation (Scheuer and Black, 2000). Thus, the morphological differences that we observed between the three females of P. heseloni likely reflect different states of bone maturation: an immature individual with unfused epiphyses (KNM-RU 2036), an older immature individual with unfused epiphyses (KNM-KPS VIII), and an adult individual with fused epiphyses (KNM-KPS III). Previous works have already suggested that the narrow ulnar head of KNM-RU 2036AJ (‘monkey-like’ morphology) is also present in juvenile chimpanzees and could represent an early stage of development (Lewis, 1969, 1971, 1989). Overall, the skeletal maturation of the RUS system (radius, ulna, and short bones) can be considered a reliable physiological age indicator in extant primates, such as macaques and chimpanzees (Nissen and Riesen, 1949; Cheverud, 1981; Hamada et al., 1998, 2003); therefore, comparisons of the overlapping carpal bones enable clarification of the developmental stages of the three P. heseloni individuals. A comparison of the carpal elements clearly shows different developmental stages between the KPS individuals and KNM-RU 2036. Although the pisiform of KNM-RU 2036 retains an open epiphysis

Pan paniscus Pan troglodytes Gorilla Pongo Hylobates Symphalangus African colobines Papio Macaca Ateles Theropithecus Nasalis Proconsul heseloni

4 Canonical axis 2 (17.45% of variance)

27

3 2 1 0

KNM-RU 2036AJ

-1 KNM-KPS U2 -2 -3 -4

-6.4

-4.8

-3.2

-1.6

0

1.6

3.2

4.8

6.4

Canonical axis 1 (77.94% of variance) Figure 8. Canonical variate analysis of the distal ulnar epiphyses of P. heseloni and extant anthropoids.

28

G. Daver, M. Nakatsukasa / Journal of Human Evolution 80 (2015) 17e33

Table 9 Results of the post-hoc test (Hotelling's T2 test). Taxonomic groups

Pan paniscus

Pan troglodytes

Gorilla

Pongo

Hylobates

Symphalangus

Papio

Theropithecus

Macaca

African colobines

Nasalis

Ateles

Pan paniscus Pan troglodytes Gorilla Pongo Hylobates Symphalangus Papio Theropithecus Macaca African colobines Nasalis Ateles Proconsul

<0.05 <0.05 n.s. <0.05 <0.05 <0.05 <0.05 <0.05 <0.05 <0.05 <0.05 <0.05

<0.05 <0.05 <0.05 <0.05 <0.05 <0.05 <0.05 <0.05 <0.05 <0.05 <0.05

<0.05 <0.05 <0.05 <0.05 <0.05 <0.05 <0.05 <0.05 <0.05 <0.05

<0.05 <0.05 <0.05 <0.05 <0.05 <0.05 <0.05 <0.05 <0.05

<0.05 <0.05 <0.05 <0.05 <0.05 <0.05 <0.05 n.s.

<0.05 <0.05 <0.05 <0.05 <0.05 <0.05 n.s.

n.s. n.s. <0.05 n.s. n.s. n.s.

n.s. <0.05 n.s. n.s. n.s.

<0.05 n.s. <0.05 n.s.

n.s. <0.05 n.s.

n.s. n.s.

n.s.

at its distal extremity (Napier and Davis, 1959), the epiphysis is completely fused in KNM-KPS III and VIII (Fig. 9). The articular borders of the carpals in KNM-RU 2036 are not well delineated, e.g., the articular surfaces of the lunate (Napier and Davis, 1959; Harrison, 1982) or the triquetral facet on the hamate, the lunate facet, and the trapezoid facet of the capitate (Morbeck, 1977a). These conditions are contrasted with the more clearly delineated surfaces on the carpals of KNM-KPS III and VIII (Daver, 2007; Fig. 9). Similar to this study, Kivell (2007) highlighted that the carpal bones from KNM-KPS III (one scaphoid, one lunate, and two capitates), KNM-KPS VIII (one capitate), and the subadult male KNM-KPS I (one scaphoid) tend to be distinguished from those belonging to KNM-RU 2036. Compared with KNM-RU 2036, KNM-KPS III is characterized by a scaphoid (C14) with a larger breadth of the body and a relatively longer lunate facet, a lunate (C22) with a longer facet for the triquetrum and narrower capitate facet and capitates (C26 and C28) as that of KNM-KPS VIII (C25), with a lower length and a longer facet for the hamate. Based on these results, Kivell (2007) suggested a possible taxonomic difference to explain the large variations she observed. However, our multivariate analyses of the distal epiphyses show that the degree of shape variation observed in P. heseloni does not exceed that of modern species, and we believe a more conservative and likely interpretation is to recognize an age-related difference between KNM-KPS III and VIII on one hand, and KNM-RU 2036 on the other hand. Implications for the positional behavior of P. heseloni In reassessing the mature condition of wrist morphology in P. heseloni, this study highlights the view that functional interpretations based on the solely immature distal antebrachial elements of KNM-RU 2036 have underestimated the forearm rotation abilities of P. heseloni. Our descriptive and quantitative approaches show that P. heseloni was capable of high degrees of mobility at the distal radioulnar joint (as illustrated by the distal ulnar surface, which is enlarged and kidney-shaped) associated with ligamentous strengthening of the joint (as illustrated by the deep ulnar fovea and the well-developed indentation on the palmar surface of the radial styloid process; Table 9). All of these characters are found in extant apes (Sarmiento, 1988) and suggest the presence of a radioulnar diarthrosis in P. heseloni. However, the presence of a clear ulnocarpal contact in P. heseloni refutes the hypothesis of a semilunar meniscus as in Pan and Hylobates, the only hominoids who share long and slender ulnar styloid processes with P. heseloni (Sarmiento, 1988; Lewis, 1989). In this regard, P. heseloni likely did not have the ligamentous strengthening that permits stability during rapid forearm rotation and resulting oscillations of the ulnar styloid process. Therefore, this study

confirms that forearm rotation in P. heseloni primarily functions under weight-bearing conditions as in quadrupedal nonhominoid primates (i.e., digitigrade, semidigitigrade, and palmigrade primates), as suggested by radiocarpal facets that are almost coplanar, a rounded lunate facet, and a long styloid process that contacts the carpus; Table 6; Fig. 3). The conjoint presence of an incipient radioulnar diarthrosis and an ulnotriquetral joint in an extinct primate is not so surprising since these conjoint structures also characterize some lorisines and to a lesser degree chimpanzees and gibbons (Cartmill and Milton, 1977; Lewis, 1989). Behaviorally, these taxa share a propensity for climbing activities and bridging involving little or no leaping or cursoriality (Cartmill and Milton, 1977; Sarmiento, 1988). In this regard, Ateles is exceptional among climbing primates since they do not display a distal radioulnar diarthrosis and have a massive ulnar styloid process articulating the triquetrum. However, they exhibit other convergent morphological traits with hominoids and lorisines in reducing dramatically the ulnotriquetral contact by intercalated soft tissue on the medial half of the triquetral surface for the styloid process (Youlatos, 1996). This observation, in addition to a lack of ulnopisiform contact, prompted Youlatos (1996: 196) to describe the ateline wrist as a “mosaic of features associated with enhanced mobility, as well as stability.” Therefore, the fact that the ulnae of KPS show osteological correlates of wrist use under weight-bearing conditions (presence of ulnotriquetral joint) and a facilitation of forearm rotation (radioulnar diarthrosis) is not antinomic and evokes the morphology of an arboreal primate involved in climbing activities and that shares a distal radioulnar joint close to those seen in extant hominoids. In highlighting the co-occurrence of these two functions in P. heseloni, our results are consistent with previous studies, which suggest that the proximal radioulnar joint of P. heseloni was mainly stable in full pronation as in all quadrupedal monkeys, but capable of high ranges of forearm rotation as in apes and to a degree likely higher than large platyrrhines (Napier and Davis, 1959; Morbeck, 1972, 1976; McHenry and Corruccini, 1975; Feldesman, 1982; Walker and Pickford, 1983; Rose, 1983, 1988, 1993, 1994, 1997; Senut, 1989). These results are of particular interest since the wrist is classically described as an especially sensitive marker of locomotor adaptations in primates, including quadrupedalism (i.e., knuckle-walking, digitigrady, palmigrady), suspension, and vertical € n and Ziemer, 1973; clinging (e.g., Tuttle, 1969b; Lewis, 1971; Scho Jenkins and Fleagle, 1975; Jenkins, 1981; Hamrick, 1996; Richmond and Strait, 2000). Previous comparative and functional studies of the overall postcranial skeleton have highlighted morphological affinities between P. heseloni and more habitually pronograde monkeys, especially those engaged in cursoriality and leaping. Proconsul heseloni

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29

Figure 9. Comparative morphology of some carpal bones from the individuals KNM-KPS III, KNM-KPS VIII, and KNM-RU 2036: for KNM-KPS III: KNM-KPS C34, left pisiform in lateral view; KNM-KPS C23, right lunate in medial view; KNM-KPS C26, left capitate in lateral view; and KNM-KPS C12, left hamate in medial view. For KNM-KPS VIII: KNM-KPS C36, left pisiform in lateral view; KNM-KPS C24, right lunate in medial view; and KNM-KPS C27 right capitate in lateral view (inversed). For KNM-RU 2036: KNM-RU 2036O, left pisiform in lateral view; KNM-RU 2036P, left lunate in medial view (reversed); KNM-RU 2036M, left capitate in lateral view; and KNM-RU 2036L left hamate in medial view. Characters; 1, the presence of a secondary center of ossification; 2, accentuated articular borders for the triquetrum on the lunate; 3, the accentuated border for the lunate on the capitates; and 4, the accentuated border of the triquetrum on the hamate. Scale bar, 10 mm.

displays limbs of nearly equal length as in cercopithecids (Walker and Pickford, 1983; Rose, 1993). The lumbar vertebral column is long and flexible, the pelvis is narrow, and presumably so was the thorax (Walker and Pickford, 1983; Rose, 1993; Ward, 1997). The ischium shows no evidence of callosity-bearing ischial tuberosities, implying sitting and sleeping behaviors similar to large platyrrhines, rather than to other anthropoids (Rose, 1993; Ward, 1993). Scapulae are positioned laterally on the thorax and most resemble colobines and large platyrrhines in their morphology (Rose, 1993; Ward, 1997). The humeral shaft is retroflexed (Rose, 1983), and the manual and pedal phalanges are quite stout and less curved

than in apes (Begun et al., 1994). The proximal ends of the proximal phalanges are slightly dorsally positioned as in palmigrade quadrupeds. Other evidence from the hindlimb of P. heseloni also supports habitual pronogrady, such as the reduced width of the acetabular lunate surfaces (Ward, 1997). The femoral head resembles that of arboreal colobines. The rest of the foot is quite similar to that of arboreal nonhominoids (Rose, 1993). These functional features are indicators of a basically quadrupedal, arboreal positional repertoire. Nevertheless, as for the distal radioulnar joint, hominoid-like features point to cautious climbing behaviors. Hence, like extant cautious climbers, P. heseloni was also

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able to produce powerful grasping at the hands and feet and a high degree of flexion of the thumb (Sarmiento, 1983; Langdon, 1986; Rose, 1992, 1993, 1994; Begun et al., 1994; Berillon, 2000), high degrees of ulnar deviation of the wrist (Beard et al., 1986), more efficient flexion-extension of the hip and knees and rotation of the legs thanks to hamstrings muscles that inserts on a uniquely long ischium (Ward, 1993, 1995; Rose, 1993, 1994; Ward, 1997; Bacon, 2001), high degree of hindlimb abduction at the thigh (Ward, 1992; Bacon, 2001), and high degrees of ab-adduction at the talocrural joint (Rose, 1993). All of these enhancements of joint mobility, combined with the absence of an external tail, indicate that P. heseloni likely maintained its balance by using powerful grasping and high degrees of joint mobility. These are features typical of extant cautious climbers that frequently use bridging behaviors (Cartmill and Milton, 1977; Ward et al., 1991; Nakatsukasa et al., 2003). Evidence from the morphology of the semicircular canals also indicates that P. heseloni was likely a slow, medium-sized quadruped (Ryan et al., 2012). Therefore, the present study of the distal radial and ulnar epiphyses of KPS implies a functional compromise between arboreal quadrupedalism and cautious climbing behaviors (including bridging sensu Cartmill and Milton, 1977), which is also indicated by the overall morphology of the postcranium of P. heseloni. To sum up, the total evidence supports the inference that P. heseloni was more adapted to nonstereotyped and sluggish pronograde climbing and bridging than previously expected and thus should not be regarded as a generalized arboreal quadruped. Evolutionary implications In showing that the wrist of P. heseloni is close to that of extant apes in certain aspects and particularly gibbons, this study strengthens the idea that some aspects of the functional morphology of P. heseloni recall that of extant apes. Even if P. heseloni differs from extant apes by using a quadrupedalism that precludes any intensive use of their specialized form of locomotion (i.e., suspension, brachiation, orthograde climbing, or knuckle-walking) (Ward, 2007), this study strongly supports that P. heseloni remains a good model for investigating the emergence of the locomotor specializations of extant apes as well as those of Miocene hominoids. Our analysis of the forearm bones from KPS leads us to identify the oldest occurrence of an incipient distal radioulnar diarthrosis on a Miocene hominoid. Despite the poor state of preservation, a distal radioulnar diarthrosis is also suggested in Oreopithecus (ca. 7e10 Ma) by the presence of a large and bifaceted ulnar head (Sarmiento, 1987). Additionally, a distal radioulnar diarthrosis may have been identified in Proconsul major at 19e20 Ma (Nengo and Rae, 1992), but this conclusion is based on a specimen from Songhor (KNM-SO 22734) of uncertain identification (Walker, 1997). Because the radioulnar diarthrosis in P. heseloni is associated with an ulnocarpal joint, we have the opportunity to reassess the function of this latter joint in other Miocene hominoids. The presence of an ulnocarpal joint has been unequivoqually identified in P. nyanzae (Beard et al., 1986) and Equatorius (Sherwood et al., 2002), and indicates that these fossil primates like P. heseloni were characterized by i) the absence of stabilization during rapid forearm rotation; ii) more stability of the wrist under weight-bearing conditions; and iii) restricted radioulnar deviation of the proximal carpal row as in quadrupedal nonhominoid anthropoids. Additionally, the present study demonstrates that the emergence of a radioulnar diarthrosis preceded the oldest occurrence of the ulnar retreat observed in the Miocene hominoid, Pierolapithecus (ca. 12 Ma), by at least six million years. Although the loss of ulnocarpal contact in Pierolapithecus was primarily associated with higher ranges of supination and ulnar deviation (Moya-Sola et al., 2004), it now seems clear from the

descriptions of the KPS fossils that P. heseloni had already developed the capability of a high degree of supination thanks to the presence of an incipient distal radioulnar diarthrosis. However, the ulnar retreat identified in Pierolapithecus illustrates a more extensive use of forearm rotation than in P. heseloni, accompanied by a reduction of weight support by the ulnae and potentially greater mediolateral mobility of the proximal carpal joint. The aforementioned features are consistent with the other ape-like traits of Pierolapithecus (broad and shallow thorax, a shift of the scapula onto the back, a stiff lumbar region) that have been functionally correlated with torsoorthograde climbing (Moy a-Sol a et al., 2004; Almecija et al., 2009). Thus, it appears that the locomotor adaptations of P. heseloni, P. nyanzae, and Equatorius, compared with those of Pierolapithecus, might represent a prerequisite for the emergence of orthograde climbing in Miocene hominoids and, subsequently, the locomotor adaptations that characterize modern apes. Two major competing models of hominoid differentiation have been proposed. First, the high levels of activities of the rotator muscles of the forearm in selected apes (four chimpanzees and two gibbons) in a variety of behaviors led Stern and Larson (2001) to support the hypothesis that hang-feeding might represent the fundamental positional adaptation of hominoids that was responsible for their differentiation. Such a feeding behavior allows an individual to utilize a larger volume from terminal branches without changing supports (Grand, 1972). The second model states that the numerous craniodental and locomotor features common to hominoids, some nonhominoid primates (colobines, atelines, lorisines, and paleopropithecines), and some non-primate mammals (sloths) highlight a strong link between an increase in body size, cautious climbing, and folivory (Sarmiento, 1988, 1995). The present study provides support for Sarmiento's model of hominoid differentiation by demonstrating that an early Miocene hominoid of medium-size such as P. heseloni was able to move cautiously on discontinuous, large, and variably oriented branches. In his model, Sarmiento (1995) also explains that hominoids that had just begun to differentiate from cercopithecoids cannot be expected to show all diagnostic traits of extant hominoids. In this respect, the consensually accepted frugivory (and not folivory as expected in Sarmiento's model) of P. heseloni (Kay and Ungar, 1997; Walker, 1997) and its general quadrupedal pattern, illustrate that this fossil primate may represent one of the earliest stages of the differentiation of the hominoid clade. Conclusions This analysis provides a reassessment of the morphological variation of the radial and ulnar distal epiphyses in P. heseloni by i) describing the seven distal antebrachial epiphyses from the individuals KNM-KPS III (adult) and KNM-KPS VIII (immature) from the Kaswanga Primate Site (Rusinga Island, Kenya), and ii) by comparing these with the distal antebrachial epiphyses of the holotype immature skeleton, KNM-RU 2036. Three main findings are described. First, we highlight that the distal antebrachial bones from both KPS individuals (and particularly KNM-KPS III) differ from those of KNM-RU 2036AJ by i) larger articular surfaces, ii) articular borders that are sharper, and iii) relief for ligament attachments that are more developed. These characters suggest that the stages of bone maturation of KNM-KPS VIII and III are more advanced compared with that of KNM-RU 2036AJ. Additionally, we show that the more mature morphology of the KPS individuals allows identification of an incipient distal radioulnar diarthrosis, a functional adaptation typical of extant apes and lorisines, which permits high ranges of mobility and better ligamentous support of the wrist during forearm rotation. Because the

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diarthrosis in P. heseloni is part of a functional complex that reflects the use of cautious pronograde climbing and bridging, this study suggests that this fossil primate should no longer be regarded as a generalized arboreal quadruped but instead as a specialized cautious pronograde climber. By providing the oldest evidence of a distal radioulnar joint in an early Miocene hominoid, this study provides support for Sarmiento's model of hominoid differentiation that highlights the role of cautious climbing as a prerequisite for the emergence of positional adaptations in apes. Acknowledgments On this occasion, we greatly acknowledge Emma Mbua, Alan Walker, and Mark Teaford for their permission to analyze the original specimens of Proconsul. We thank the Office of the President of the Republic of Kenya for permission to perform research in Kenya (Research Permit n MOEST/13/001/34C 418). We are grateful to the curatorial staff in the following institutions: Museum national d'Histoire naturelle of Paris, National Museums of Kenya,
e Royal d'Afrique Centrale of Tervuren, Naturalis Biodiversity Muse Center of Leiden, and Anthropologische Institut und Museum of the Zurich-Irchel University. We are also very grateful to Drs. A. Balzeau, S. Pavard, and J.-R. Boisserie and anonymous reviewers, the associate editor, and the editor-in-chief for thoughtful comments on the manuscript. This study was funded by a ‘Louis Forest’ science grant awarded by JSPS Kakenhi 25257408 (to MN), the Chancellery
te
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