1. TITLE PAGE Title: Modeling the dental development of fossil

advertisement
1
1. TITLE PAGE
2
Title: Modeling the dental development of fossil hominins through the inhibitory cascade
3
KES SCHROER1,2 and BERNARD WOOD3,4
4
1
5
Dartmouth, 6047 Silsby Hall, Hanover NH 03755, USA, 3Center for the Advanced Study of
6
Hominid Paleobiology, Department of Anthropology, The George Washington University, 2110
7
G St NW, Washington DC 20052, USA, 4Human Origins Program, National Museum of Natural
8
History, Smithsonian Institution.
9
Corresponding author: kes.schroer@gmail.com
10
11
Neukom Institute for Computational Science, Dartmouth, 2Department of Anthropology,
2. SUMMARY
The inhibitory cascade is a mathematical model for interpreting the relative size of the
12
occlusal surfaces of mammalian molars in terms of developmental mechanisms. The cascade is
13
derived from experimental studies of mouse molars developed in culture, and has been tested and
14
applied to the dentitions of rodents, ungulates, carnivores, and platyrrhines. Results from such
15
applications have provided new information regarding the origins of plesiomorphic traits in
16
mammalian clade and how derived morphologies may arise. In this study we apply the inhibitory
17
cascade model to the postcanine dentition of a sample of Old World primates that includes fossil
18
hominins. The results of this study suggest that the inhibitory cascade (i.e., M1<M2<M3)
19
describes the relative sizes of the molar occlusal areas of Old World primates and is likely the
20
plesiomorphic condition for this clade. Within that clade, whereas most Old World monkeys
21
have a M1<M2<M3 pattern, most apes have a M1<M2≈M3 pattern. This modified cascade
22
suggests that greater levels of inhibition (or less activation) are acting on the posterior molars of
23
apes, thus facilitating the reduction of M3s within the apes. With the exception of the baboon
1
24
genus Papio, extant congeners typically share the same molar inhibitory cascade. The differences
25
in the relative size relationships observed in the molar and premolar-molar cascades of the
26
species included in the fossil hominin genus Paranthropus suggest that although large postcanine
27
teeth are a shared derived trait within this genus, the developmental basis for postcanine
28
megadontia may not be the same in these two Paranthropus taxa. Our results showthat
29
phenotypic characters like postcanine megadontia may not reflect common development. .
30
3. KEYWORDS
31
Fossil hominin, human evolution, inhibitory cascade, Paranthropus, monophyly, primates,
32
postcanine teeth, molar size.
33
4. INTRODUCTION
34
Evolutionary developmental biologists have begun to determine the regulatory pathways
35
that govern the process of tooth formation and the details of occlusal morphology (Jernvall et al.,
36
2000; Jernvall and Thesleff, 2000, 2012; Salazar-Ciudad and Jernvall, 2002, 2004, 2010;
37
Tummers and Thesleff, 2003, 2009; Jarvinen et al., 2006; Munne et al., 2009; Renvoise et al.,
38
2009; Michon et al., 2010). This research has helped unravel the complex relationships between
39
the genotype and phenotype of the dentition (Arnold, 1992; Hall, 2003; Polly, 2008) and it has
40
shown how molecular processes can influence macroevolutionary trends (Peterson et al., 2007;
41
Raff, 2007). In particular, understanding the mechanisms underlying tooth development helps
42
quantify potential constraints on tooth evolvability and helps understand how adaptation can
43
result in the modification of regulatory pathways (Renaud et al., 2011; Felix, 2012; Asahara,
44
2013; Bernal et al., 2013; Halliday and Goswami, 2013).
45
46
Fossils are difficult to study within a developmental context. However, the inhibitory
cascade model proposed by Kavanagh and colleagues (2007) allows researchers to generate
2
47
hypotheses about how regulatory pathways might have influenced evolutionary trends seen in the
48
postcanine dentition of mammals, including hominins. The inhibitory cascade model is the result
49
of Kavanagh and colleagues’ use of cell culture techniques to investigate mouse dental
50
development. They found that when the lower molars of Mus musculus were isolated from their
51
posterior tail, the rate of initiation of posterior molars was increased and the posterior molars
52
were enlarged. Kavanagh and colleagues hypothesized that the net balance between genetic
53
activation and inhibition during dental development determines the relative size of the teeth in
54
the molar row. Kavanagh and colleague’s simplified model to describe the genotypic-phenotypic
55
relationship between molar position and molar size is:
56
y=1+[(a–i)/i](x–1),
57
where y is the relative molar size estimated from occlusal area, x is the position of the molar in
58
the tooth row, a is the strength of activation, and i is the strength of inhibition.
59
Because teeth develop in sequence, the inhibitory cascade model can be used to predict
60
the relative size of the teeth in the molar row. For a typical mammal the above equation predicts
61
that M1=1, M2=a/i, and M3=2a/i-1). The model also predicts a slope of 2.0 and an intercept of -
62
1.0 to describe the ratios between the M2:M1 and M3:M1 occlusal areas. Expressed in another
63
way, the occlusal area of M2 will consistently be 1/3rd the total occlusal area of the molar row
64
since M2/(M1+M2+M3)=(a/i)/[1+a/i +(2a/i–1)]=1/3 (Kavanagh et al., 2007). Weak inhibition
65
(i.e., high a/i) by M1 on the posterior molars results in a molar row that increases in size from
66
anterior to posterior (i.e., the ratio between occlusal areas is >1). Conversely if the ratio is <1,
67
this suggests strong inhibition and results in a molar row that decreases in size from anterior to
68
posterior. A summary schematic of the inhibitory cascade model is provided in Figure 1.
3
69
The inhibitory cascade model also has the potential to help in phylogenetic
70
reconstruction. By applying the model to a large set of fossil and extant mammals, researchers
71
have demonstrated that the relative sizes of most mammalian molars follow the predictions of the
72
inhibitory cascade and may be symplesiomorphic for relative molar sizes in this clade (Halliday
73
and Goswami, 2013). Differences in the relative occlusal areas of postcanine tooth crowns can
74
differentiate the major radiations of mammals (Wilson et al., 2012), and the evolution of
75
specialized teeth such as carnassials is linked with departures from the symplesiomorphic
76
condition of the inhibitory cascade (Asahara, 2013; Halliday and Goswami, 2013).
77
Preliminary analyses suggest that primates generally conform to the inhibitory cascade
78
(Polly, 2007; Halliday and Goswami, 2013) and an in-depth study of platyrrhine (New World)
79
primates suggests that when phylogeny is taken into account their relative occlusal areas do not
80
differ significantly from the pattern predicted by the inhibitory cascade model (Bernal et al.,
81
2013). This study applies the inhibitory cascade model to a large sample of catarrhine (Old
82
World) primates that includes fossil hominins. With respect to the molars, we test the hypotheses
83
that most primate groups will have plesiomorphic molar proportions, and that species with
84
specialized dental morphologies will depart from the symplesiomorphic condition. We also test
85
the hypothesis that closely related taxa (e.g., sister taxa) will either share the plesiomorphic
86
condition or depart from it in similar ways.
87
This study also extends the inhibitory cascade model to the premolar tooth row, although
88
the results of this second cascade should be considered preliminary. Premolars are a different
89
developmental class of teeth from molars (Avery, 2001; Ash and Nelson, 2003), and unlike
90
molars, premolars emerge posteriorly to anteriorly in primates (Swindler, 2002). Yet, premolars
91
are functionally similar to molars (Lucas, 2004) and their developmental initiation and crown
4
92
completion patterns are the same as in molars (Swindler, 2002). Evidence of integrative modules
93
in the postcanine dentitions of hominoids (Gomez-Robles and Polly, 2012) and papionins
94
(Hlusko and Mahaney, 2009) suggest links between premolar and molar development. A recent
95
examination of rodent clades with and without the last premolar found that first molar (M1)
96
variation increased in the absence of the P4, suggesting that the presence of a P4 constrains the
97
morphology of the M1 in the way that the M1 inhibits the size of the M2 and M3 in the inhibitory
98
cascade (Labonne et al., 2012). Furthermore, the phenotypic similarity between the molarized
99
posterior premolars and the molars in the species included in the hominin genus Paranthropus
100
(Robinson, 1956; Butler, 1997, 2000; Jernvall et al., 2008) also suggests similarities in genetic
101
control. In this study, we test whether the relative sizes of the series P4, M1, and M2 can be
102
inferred from an inhibitory cascade model.
103
5. MAIN BODY
104
Materials and Methods
105
1. Sample composition
106
In order to provide a comparative context for the analysis of the species within the
107
hominin genus Paranthropus (aka “robust” australopiths) our sample deliberately included Old
108
World monkeys (i.e., cercopithecoids; Cercocebus, Macaca, Papio, and Presbytis), and apes
109
(i.e., hominoids; Hylobates, Gorilla, Pan, and Pongo) genera that have been used previously as
110
morphological and ecological analogues for the postcanine megadontia and robust craniofacial
111
morphology seen in that genus (Strait et al., 2007; Vogel et al., 2008; Cerling et al., 2011;
112
Daegling et al., 2011; Wood and Schroer, 2012).
113
114
Morphological evidence supports the hypothesis that the “robust” australopiths are a
clade recognized as the genus Paranthropus (Wood and Chamberlain, 1986, 1987; Wood, 1988;
5
115
Strait et al., 1997; Wood and Richmond, 2000; Kimbel et al., 2004; Strait and Grine, 2004).
116
However, there is debate about whether the species presently included within this genus are
117
sister taxa (Wood, 1988; McCollum, 1999; Constantino and Wood, 2007; Wood and Schroer,
118
2012; Foley, 2013). The temporally-earlier of the two main species within Paranthropus,
119
Paranthropus boisei, has several derived features compared to Paranthropus robustus, which the
120
current fossil record suggests is nearly half a million years younger (Wood and Richmond,
121
2000). The morphology of P. boisei is so derived that when the first fossil evidence of the
122
species was discovered, its morphology warranted the formation of a new genus, Zinjanthropus
123
(Leakey et al., 1964). In this study, we maintain the taxonomic designations P. boisei and P.
124
robustus to highlight their overall similarities, but we use the inhibitory cascade model to test the
125
hypothesis of “robust” australopith monophyly.
126
In addition to Paranthropus, two other fossil hominin genera were included in the analysis:
127
Homo, the genus that includes modern humans, and Australopithecus, the likely ancestral clade
128
of both Paranthropus and Homo (Strait et al., 1997). Because there is much debate about the
129
taxonomic significance of the variation seen in early Homo (e.g. Miller 1991, 2000; Wood, 1992;
130
Kramer, 1993; Kramer et al., 1995; Lieberman et al., 1996; Kennedy, 1999; Wood and Collard,
131
1999a,b; Anton, 2003; Gilbert et al., 2003; Leakey et al., 2012; Lordkipanidze et al., 2013)
132
specimens of Homo were divided into just two inclusive groups. This first, Homo habilis sensu
133
lato, includes some specimens that have been referred to Homo rudolfensis (e.g., Lieberman et
134
al., 1996; Wood and Collard, 1999a,b; Strait and Grine, 2004; Leakey et al., 2012). The second
135
group, Homo erectus sensu lato, includes some specimens that have been referred to Homo
136
ergaster (e.g., Wood and Collard, 1999a,b; Wood, 1992; Wood and Richmond, 2000, Strait and
137
Grine, 2004). This group also includes the southern African specimen SK 15 and the Dmanisi
6
138
fossil hominins, which were initially referred to Homo georgicus (Gabounia et al., 2002), but
139
more recently they have been assigned to Homo erectus (Lordkipanidze et al., 2013). The
140
specimen numbers and the sources of measurements for the fossil hominins are given in Table
141
S1.2. Materials and methods
142
Lower jaws of the extant primate genera were obtained from the collections of the
143
American Museum of Natural History in New York City, National Museum of Natural History
144
in Washington DC, and Natural History Museum in London. All specimens were adult and from
145
wild populations. The species samples were sex balanced. The representative species of each
146
genus are equally sampled, except in the case of Pan where specimens of Pan paniscus were
147
unavailable for study.
148
Measurements of fossil hominin postcanine teeth were obtained from precision casts in
149
the collections at The George Washington University and the University of Arkansas, with the
150
balance taken from the literature. All specimens were from individuals with erupted M3s, but sex
151
was not controlled. The representative species of each genus are equally sampled
152
Only individuals with complete M1-M3 or P4-M2 series were analyzed. Specimens with
153
occlusal wear that masked the identification of individual cusps, or with interproximal wear that
154
affected >20% of the occlusal margin, were not included in the extant sample. For teeth with
155
moderate interstitial wear, the worn margin was reconstructed by approximating the curvature of
156
the margin from overall crown shape (Wood and Uytterschaut, 1987; Bailey and Lynch, 2005).
157
Specimens were photographed using a Canon Digital Rebel XT camera fitted with a 60
158
mm macro lens. A scale was set and leveled in the occlusal plane of the teeth, and levels on the
159
camera and photography stand were used to make sure that the occlusal plane was parallel to the
160
lens of the camera. Maximum mesiodistal and buccolingual diameters for each postcanine tooth
7
161
were obtained via scaled measurements in TPSDig (Figure S1; Rohlf, 2009), and occlusal areas
162
were computed by multiplying these diameters (Kavanagh et al., 2007; Polly, 2007; Wilson et
163
al., 2012; Halliday and Goswami, 2013). Mesiodistal and buccolingual diameters for all extant
164
primate and fossil hominin specimens are available at
165
http://dx.doi.org/10.6084/m9.figshare.1181983.
166
To investigate intra-observer error, 45 individuals (i.e., c. 20 % of the extant sample)
167
were drawn from among all of the extant taxa in the study and re-measured two months after the
168
initial set of measurements. Intra-observer error for linear measurements was ±0.4 mm.
169
3. Analysis
170
Two different postcanine cascades, the standard M1-M3 and the P4-M2, were tested
171
against the murine inhibitory cascade model. We used two inter-tooth ratios for each analysis,
172
M2:M1 and M3:M1 for the molar cascade and M1:P4 and M2:P4 for the premolar-molar cascade.
173
Reduced major axis regression (RMA) was used to examine the nature of any
174
correlations between relative occlusal areas. There are reservations about the use of RMAs for
175
anything other than the ratios of the standard deviations of y on x (Smith, 2009), but RMA is
176
used in the inhibitory cascade model because a single line defines the ratio between x and y (i.e.,
177
the relationship of the data is symmetrical). Data were considered to falsify the predictions of the
178
inhibitory cascade model when the 95% confidence interval of the slope does not include 2.00.
179
Because RMA regressions have the tendency to drive small sample sizes toward a slope of 1, the
180
use of the RMA makes it more likely that the prediction that groups will fall within the
181
boundaries of the inhibitory cascade model will be falsified.
182
183
RMA regressions were performed in software developed in the C programming language
with standard linear regression error estimates (Bohonak, 2004). Data were bootstrapped 1000
8
184
times and the resulting regression compared to the predictions of the murine inhibitory cascade.
185
Even when the significance values for r2 were low, regressions with confidence intervals that
186
included the 2.0 slope and -1.0 intercept predicted by the inhibitory cascade model were
187
determined “validated” as is prior practice (Renvoise et al., 2009; Wilson et al., 2012; Halliday
188
and Goswami, 2013).
189
Means and standard deviations of the occlusal areas of each postcanine tooth, P4-M3, are
190
reported for the extant genera in Table S2. The individual measurements from each fossil tooth
191
are given in Table S3. Results of a MANOVA conducted in R indicated that the ratios of
192
occlusal areas for all taxa are significantly distinct from one another (Table S4). A Pillai trace
193
was applied to protect against Type I errors for small samples. Small samples were of a
194
particular concern for the interpretation of the slopes of P. boisei and P. robustus, and Student’s
195
t-test was employed to test whether the slopes of the regression lines for the relative molar sizes
196
of P. boisei and P. robustus were statistically different (Table S5).
197
Results
198
1. RMA regressions
199
In most extant primates, RMA regressions of the molar ratios at both the species and
200
genus levels have 95% confidence intervals that include the slope and intercept predicted by the
201
murine inhibitory cascade (Table 1). Thus, based on the results of this analysis, the inhibitory
202
cascade model can be generally applied to the extant primates included in this study. The
203
exceptions among extant primates include Cercopithecus, which is not validated by the model at
204
either the species or genus level, and Papio ursinus, which unlike its congeners does not fit the
205
model. All other extant congeners share similar fits to the inhibitory cascade.
9
206
Among the fossil hominin genera, the molar ratios of Australopithecus and Homo
207
conform to the predictions of the murine inhibitory cascade model at the species level. At the
208
genus level, the relationship between the occlusal areas of the molars of Homo can be described
209
by the intercept of the inhibitory cascade but not by its slope. The maximum confidence interval
210
of the slope of Homo in this study is 1.96 as opposed to the 2.00 dictated by the parameters of the
211
inhibitory cascade, which may relate to the variation observed in the relative occlusal areas of H.
212
habilis sensu lato. Within the genus Paranthropus, the congeners P. robustus and P. boisei differ
213
notably. While the relative occlusal areas of P. robustus are well described by the inhibitory
214
cascade, neither the intercept nor slope of P. boisei fit the model.
215
There is no evidence of a consistent pattern for the premolar-molar cascade among extant
216
or fossil genera (Table 2). Among the extant primates, the molarized premolars of Cercocebus fit
217
the proposed premolar-molar cascade, but the proposed premolar-molar cascade also fits some
218
taxa with no evidence of molarization (e.g., Cercopithecus mitis and Hylobates albibarbis).
219
Within Paranthropus, both P. robustus and P. boisei are considered to have molarized
220
premolars, but only P. robustus fits the proposed premolar-molar cascade.
221
2. Regression plots
222
The results of the RMA are summarized in linear regression plots of the molar cascade
223
and the proposed premolar-molar cascade. The proportions of the molar occlusal areas of extant
224
primates are weakly correlated (r2 = 0.55). The cercopithecoids in the extant sample conform to
225
the slope of murine inhibitory cascade model more closely than the hominoids (Figure 2).
226
Hominoids, including fossil hominins, have similarly-sized M2s and M3s compared to
227
cercopithecoids (Figure 3). That is, most hominoids are described by the occlusal relative size
228
order, M1<M2≈M3.
10
229
The regression of molar sizes in P. boisei differs from that of its congener P. robustus
230
(Figure 4). Whereas P. robustus shares the M1<M2<M3 pattern seen in the majority of primates
231
in this study, P. boisei is unusual because of the relative sizes of its M2s and M3s, which are
232
much larger than predicted from the occlusal area of M1. The area of the M2 is especially large
233
given the size of the M1.
234
If we accept a working hypothesis that P4 development influences the size of the M1 and
235
M2, we can report a few patterns from an examination of premolar-molar ratios. The premolar-
236
molar ratios of extant primates are very weakly correlated (r2 = 0.27). Catarrhine primates have a
237
P4-M2 relative size sequence (P4<M1<M2) that resembles that for M1-M3. At the level of the
238
superfamily, cercopithecoids tend to have premolar-molar proportions above the trajectory
239
predicted on the basis of the molars (Figure 5), whereas extant hominoids consistently fall below
240
this trajectory. This is because, when P4 crown size is normalized, cercopithecoids tend to have
241
larger M2s than hominoids. Among the fossil hominins, although Au. africanus, H. habilis s.l., H.
242
erectus s.l., and P. robustus resemble extant hominoids (Figures 6 and 7), most P. boisei
243
specimens tend to follow the cercopithecoid pattern.
244
11
245
Discussion
246
1. Molar cascade
247
The murine inhibitory cascade predicts the relative occlusal areas of extant primate
248
molars, and we suggest that it is the plesiomorphic condition for catarrhine primates. The
249
catarrhines are broadly described by a molar row in which the relative occlusal areas increase in
250
size. Hominoids tend to have more similarly-sized M2s and M3s than cercopithecoids. Based on
251
the murine experiments, this suggest that hominoids have a derived developmental pathway in
252
which there is less activation on the posterior molars, more inhibition on the posterior molars, or
253
some combination of these effects. The M1<M2≈M3 pattern may relate to the timing of the
254
emergence of the M1, which occurs later in Pan than in cercopithecoids (Kelley and Smith,
255
2003). Late emergence of the M1 may delay the initiation of posterior molars and subsequently
256
affect the final size of posterior molars. If late emergence of the M1 is the plesiomorphic
257
condition of hominoids, this would account for the reduced M3s described in several hominoid
258
lineages (Nanda, 1954; Garn, 1962, 1963; Garn et al., 1964; Frisch, 1967, 1973; Lavelle, 1970;
259
Lavelle and Moore, 1973; Mahler, 1973; Kinzey, 1984; Plavcan and Gomez, 1993; Smith, 1994;
260
Swindler, 1998; Dean and Lucas, 2009). This condition may also be the precursor to the much
261
delayed emergence of the M1 in H. erectus s.l. and later Homo (Dean et al., 2001).
262
Our null hypothesis, which is that closely-related taxa will share the same inhibitory
263
cascade, is supported by the observation that in all but one extant primate genera, congeners
264
share the same inhibitory cascade. The exception, Papio, has a complex evolutionary history
265
featuring substantial introgression (Keller et al., 2010; Jolly et al., 2011) and paraphyletic species
266
(Zinner et al., 2009). Rather than divisions along traditionally recognized species lines,
267
mitochondrial DNA studies have detected a major division between Papio groups in East and
12
268
southern Africa (Newman et al., 2004; Zinner et al., 2009). This division is also found in this
269
study, with specimens of Papio from East Africa (Papio anubis and Papio cynocephalus) sharing
270
the same inhibitory cascade, while the southern African group (Papio ursinus) did not.
271
The results from the analysis of extant primates provide a comparative context for
272
interpreting the relationships between fossil hominins. Paranthropus robustus shares the
273
plesiomorphic condition of extant primates, in which M3 is predictably the largest tooth in the
274
molar series. Conversely, P. boisei has much larger M2s than predicted by the occlusal areas of
275
the M1 and, as a taxon, has the absolutely and relatively largest M2:M1 ratio in this study. A
276
distinct M1<M2>M3 molar size sequence is rare among mammals, requiring both low inhibition
277
levels and a premature stop to M3 development (Kavanagh et al., 2007; Polly, 2007; Labonne et
278
al., 2012); such genetic constraints may be one of the determinants of the relative size of the M2
279
in P. boisei.
280
13
281
282
2. Premolar-molar cascade
There was no consistent evidence of a premolar-molar cascade among the primate genera
283
and species examined here, even within taxa described by molarized premolars. However, when
284
the data are considered at the superfamily level, there is a difference in the P4-M2 relative size
285
relationships between cercopithecoids and hominoids. Cercopithecoid taxa tend to fall above the
286
predictions of this model, whereas the hominoid taxa tend to fall below this prediction. That is to
287
say, for similar M1:P4 occlusal area ratios, cercopithecoids tend to have larger M2s than
288
hominoids. This is consistent with the results of the molar cascade, which suggests that
289
hominoids have reduced M3s compared to cercopithecoids. Rather than assume that the
290
principles of the molar cascade can be applied to premolars and molars without any
291
modification, experimental work using mouse mutants with artificially induced premolars
292
(Peterkova et al., 2005; Klein et al., 2006; D’Souza et al., 2007) could help develop a model
293
specific to the P4-M2 sequence. This would also help researchers better understand the factors
294
that contribute to premolar molarization.
295
6. CONCLUSION
296
This study is an example of how models derived from the principles of evolutionary
297
development can help improve our understanding of macroevolutionary trends. By determining
298
how postcanine crown area may be influenced by an inhibitory cascade, it is possible to evaluate
299
dependent relationships between dental morphologies that may otherwise appear as independent
300
traits. Thus, on the basis of the inhibitory cascade, the taxa within the fossil hominin genus
301
Paranthropus do not share the same molar size relationships. Relative molar size is not
302
consistent with the hypothesis of Paranthropus monophyly. This study adds to other
303
morphological differences seen in the megadont postcanine dentitions of P. boisei and P.
14
304
robustus (Wood, 1988; Suwa et al., 1994, McCollum, 1999) and suggests that it may no longer
305
be prudent to assume that postcanine megadontia is a synapomorphy of Paranthropus. If the
306
results of the analyses conducted here are confirmed, they affect our understanding of the
307
evolutionary significance of postcanine megadontia and premolar molarization. Developmental
308
biology continues to illuminate the details of the complex relationships between genotype and
309
phenotype, and by doing so it improves our ability to generate more reliable hypotheses about
310
early hominin taxonomy and phylogeny.
311
7. ACKNOWLEDGEMENTS
312
The manuscript was greatly improved by comments from Drs. Patricia Hernandez, Aida Gomez-
313
Robles, and Mark Grabowski (George Washington University), Matthew Skinner (University
314
College London), Paul Constantino (Marshall University), and two anonymous reviewers. Brian
315
Richmond provided comments on an early version of the manuscript. This study was conceived
316
while under the supervision of Dr. Jukka Jernvall (University of Helsinki) and benefited from his
317
comments. Dr. Peter Ungar (University of Arkansas) provided access to many fossil casts.
318
Access to extant species was made possible through Linda Gordon, Darrin Lunde, and Dr.
319
Matthew Tocheri (NMNH), Eileen Westwig (AMNH), and Roberto Portela Miguez (BMNH).
320
Kristen Ramirez (CUNY) and Christine Foltz assisted with photography. David Otten
321
(University of Arkansas), Michael Frick, Teresa Girolamo, and David Cobey provided
322
hospitality during museum visits. Funding for this research was provided by the NSF-IGERT
323
DGE-0801634, an NSF-GRF to KS, a Cosmos Club Scholars Award to KS, and a special gift
324
from the Council of Scientific Society Presidents to KS. The authors declare no conflict of
325
interest.
326
15
327
Author contributions: KS conceived of the application of the inhibitory cascade to fossil
328
hominins, and BW encouraged the application of the model to reinterpreting the relationships
329
among Paranthropus taxa. BW assisted with arranging visits to extant and fossil collections. All
330
measurements and analyses were performed by KS. The initial manuscript was drafted by KS
331
with critical revisions by both authors.
332
8. REFERENCES
333
Anton, S.C., 2003. Natural history of Homo erectus. Am. J. Phys. Anthropol., 122, pp. 126-70.
334
Arnold, S.J., 1992. Constrains of phenotypic evolution. Am. Nat., 130, pp. 85-107.
335
Asahara, M., 2013. Unique inhibitory cascade pattern of molars in canids contributing to
336
their potential to evolutionary plasticity of diet. Ecol. Evol., 3, pp. 278-85.
337
338
339
340
341
Ash, M., and Nelson, S.J., 2003. The primary (deciduous) teeth. In: S.J. Nelson, ed. Wheeler’s
Dental Anatomy, Physiology and Occlusion. St. Louis: Elsevier.
Avery, D.M., 2001. The Plio-Pleistocene vegetation and climate of Sterkfontein and
Swartkrans, South Africa, based on micromammals. J. Hum. Evol., 41, pp. 113-32.
Bailey, S.E., and Lynch, J.M., 2005. Diagnostic differences in mandibular P4 shape between
342
Neandertals and anatomically modern humans. Am. J. Phys. Anthropol., 126, pp. 268-
343
77.
344
345
346
Bernal, V., Gonzalez, P.N., and Perez, S.I., 2013. Developmental processes, evolvability, and
dental diversification of New World monkeys. Evol. Biol., 40, pp. 532-41.
Bohonak, A.J., and van der Linde, K., 2004. RMA: software for reduced major axis
347
regression, Java version. Available at: <www.kimvdlinde.com/professional/rma.html>
348
[Accessed 20 January 2014].
349
16
350
351
Butler, P.M., 1997. An alternative hypothesis on the origin of docodont molar teeth. J.
Vert. Paleontol., 17, pp. 435-9.
352
Butler, P.M., 2000. The evolution of tooth shape and tooth function in primates. In:
353
M.F. Teaford, M.M. Smith, and M.W.J. Ferguson, eds. Development,
354
Function and Evolution of Teeth. Cambridge: Cambridge University Press, pp.
355
201-11.
356
Cerling, T.E., Mbua, E., Kirera, F.M., et al., 2011. Diet of Paranthropus boisei in the early
357
Pleistocene of East Africa. P. Natl. Acad. Sci. USA, 108, pp. 9337-41.
358
Constantino, P.J., and Wood, B., 2007. The evolution of Zinjanthropus boisei. Evol.
359
360
Anthropol., 16, pp. 49–62.
D’Souza, R.N., and Klein, O.D., 2007. Unraveling the molecular mechanisms that lead to
361
supernumerary teeth in mice and men: current concepts and novel approaches.
362
Cells, Tissues, Organs, 186, pp. 60-9.
363
Daegling, D.J., McGraw, W.S., Ungar, P.S., et al., 2011. Hard-object feeding in sooty
364
mangabeys (Cercocebus atys) and interpretation of early hominin feeding ecology.
365
PLoS ONE, 6, e23095.
366
367
368
369
370
371
Dean, M.C., Leakey, M.G., Reid, D., et al. 2001. Growth processes in teeth distinguish modern
humans from Homo erectus and earlier hominins. Nature, 414, pp. 628-31.
Dean, M.C., and Lucas, V.S., 2009. Dental and skeletal growth in early fossil hominins. Ann.
Hum. Biol., 36, pp. 545-61.
Felix, M.A., 2012. Evolution in developmental phenotype space. Curr. Opin. Genetics Dev., 22,
pp. 593-9.
372
17
373
Foley, R.A., 2013. Comparative evolutionary models and the “australopiths radiations.” In: K.E.
374
Reed, J.G. Fleagle, and R.E. Leakey, eds. The Paleobiology of Australopithecus. New
375
York: Springer, pp. 163-74.
376
377
Frisch, J.E., 1967. The gibbons of the Malay peninsula and of Sumatra. Primates, 8, pp. 297310.
378
Frisch, J.E., 1973. The society and life of Japanese monkeys. Am. Anthropol., 75, pp. 2009-10.
379
Gabounia L, de Lumley M.-A.., Vekua, A., Lordkipanidze, D, and de Lumley H. 2002.
380
Discovery of a new hominid at Dmanisi (Transcaucasia, Georgia). Comptes Rendus
381
Palevol.. 1: 243-53.
382
Garn, S.M., 1962. The newer physical anthropology. Am. Anthropol., 64, pp. 917-8.
383
Garn, S.M., 1963. Physical anthropology today. Am. J. Phys. Anthropol., 21, pp. 225-6.
384
Garn, S.M., Lewis, A.B., and Kerewsky, R.S., 1964. Third molar agenesis and variation in size
385
386
387
of the remaining teeth. Nature, 201, pp. 839.
Gilbert, W.H., 2003. Homo erectus, Homo ergaster, Homo “cepranensis,” and the Daka
cranium.” J. Hum. Evol., 45, pp. 255-9.
388
Gomez-Robles, A., and Polly, P.D., 2012. Morphological integration in the hominin dentition:
389
evolutionary, developmental, and functional factors. Evolution, 66, pp. 1024-43.
390
391
392
393
394
395
Hall, B.K., 2003. Evo-devo: evolutionary developmental mechanisms. Int. J. Developmental
Biol., 47(7/8), pp. 491-6.
Halliday, T.J.D., and Goswami, A., 2013. Testing the inhibitory cascade model in Mesozoic
and Cenozoic mammaliforms. BMC Evol. Biol., 13, pp. 79.
Hlusko, L.J., and Mahaney, M.C., 2009. Quantitative genetics, pleiotropy, and morphological
integration in the dentition of Papio hamadryas. Evol. Biol., 36, pp. 5-18.
18
396
Jarvinen, E., Salazar-Ciudad, I., Birchmeier, W., et al., 2006. Continuous tooth generation in
397
mouse is induced by activated epithelial Wnt/beta-catenin signaling. P. Natl. Acad. Sci.
398
USA, 103, pp. 18627-32.
399
Jernvall, J., Gilbert, C.C., and Wright, P.C., 2008. Peculiar tooth homologies of the greater
400
bamboo lemur (Prolemur=Hapalemur simus). In: J. Fleagle and C. Gilbert, eds. Elwyn
401
Simons: A Search for Origins. New York: Springer, pp. 335-42.
402
Jernvall, J., Keränen, S.V., and Thesleff, I., 2000. Evolutionary modification of development in
403
mammalian teeth: quantifying gene expression patterns and topography. P. Natl. Acad.
404
Sci. USA, 97, pp. 14444-8.
405
406
407
408
409
Jernvall, J., and Thesleff, I. 2000. Reiterative signaling and patterning during mammalian tooth
morphogenesis. Mech. Develop., 92, pp. 19-29.
Jernvall, J. and Thesleff, I., 2012. Tooth shape formation and tooth renewal: evolving with the
same signals. Development, 139, pp. 3487-97.
Jolly, C.J., Burrell, A.S., Phillips-Conroy, J.E., Bergey, C., and Rogers, J., 2011. Kinda
410
baboons (Papio kindae) and grayfoot chacma baboons (P. ursinus griseipes) hybridize
411
in the Kafue river valley, Zambia. Am. J. Primatol., 73, pp. 291-303.
412
413
414
Kavanagh, K.D., Evans, A.R., and Jernvall, J., 2007. Predicting evolutionary patterns of
mammalian teeth from development. Nature, 449, pp. 427–32.
Keller, C., Roos, C., Groeneveld, L.F., Fischer, J., and Zinner, D., 2010. Introgressive
415
hybridization in southern African baboons shapes patterns of mtDNA variation. Am. J.
416
Phys. Anthropol., 142(1), pp. 125-36.
417
418
Kelley, J., and Smith, T.M., 2003. Age at first molar emergence in early Miocene Afropithecus
turkanensis and life-history evolution in the Hominoidea. J. Hum. Evol., 44, pp. 307-29.
19
419
Kennedy, G.E., 1999. Is “Homo rudolfensis” a valid species? J. Hum. Evol., 36, pp. 119-21.
420
Kimbel, W.H., Rak, Y., Johanson, D.C., Holloway, R.L., and Yuan, M.S., 2004. The skull of
421
422
423
Australopithecus afarensis. Oxford University Press, Oxford.
Kinzey, W.G., 1984. The dentition of the pygmy chimpanzee, Pan paniscus. In: R.L. Susman, \
ed. The Pygmy Chimpanzee. New York: Springer, pp. 65-88.
424
Klein, O.D., Minowada, G., Peterkova, R., et al., 2006. Sprouty genes control diastema tooth
425
development via bidirectional antagonism of epithelial- mesenchymal FGF signaling.
426
Dev. Cell, 11(2), pp. 181-90.
427
428
429
Kramer, A., 1993. Human taxonomic diversity in the Pleistocene: Does Homo erectus represent
multiple hominid species? Am. J. Phys. Anthropol., 91, pp. 161-71.
Kramer, A., Donnelly, S,M,, Kidder, J.H., Ousley, S.D., and Olah, S.M., 1995. Craniometric
430
variation in large-bodied hominoids: testing the single-species hypothesis for Homo
431
habilis. J. Hum. Evol., 29, pp. 443-62.
432
433
Labonne, G., Laffont, R., Renvoise, E., et al., 2012. When less means more: evolutionary and
developmental hypotheses in rodent molars. J. Evolution. Biol., 25, pp. 2102-11.
434
Lavelle, C.L.B., 1970. Analysis of attrition in adult human molars. J. Dent. Res., 49, pp. 822-8.
435
Lavelle, C.L.B., and Moore, W.J., 1973. The incidence of agenesis and polygenesis in the
436
437
438
primate dentition. Am. J. Phys. Anthropol., 38(3), pp. 671-9.
Leakey, L.S., Tobias, P.V., and Napier, J.R., 1964. A new species of the genus Homo from
Olduvai Gorge. Nature, 202(4927), pp. 7-9.
439
Leakey, M.G., Spoor, F., Dean, M.C., et al., 2012. New fossils from Koobi Fora in northern
440
Kenya confirm taxonomic diversity in early Homo. Nature, 488, pp. 201-4.
441
20
442
Lieberman, D.E., Wood, B.A., and Pilbeam, D.R., 1996. Homoplasy and early Homo : an
443
analysis of the evolutionary relationships of H . habilis sensu stricto and H. rudolfensis.
444
J. Hum. Evol., 30, 97-120.
445
Lordkipanidze, D., Ponce de Leon, M.S., Margvelashvili, A., et al., 2013. A complete skull from
446
Dmanisi, Georgia, and the Evolutionary Biology of Early Homo. Science, 342, pp. 326-
447
331.
448
449
Lucas, P., 2004. Dental Functional Morphology: How Teeth Work. Cambridge: Cambridge
University Press.
450
Mahler, P., 1973. Metric variation in the pongid dentition. Ph.D. University of Michigan.
451
Michon, F., Tummers, M., Kyyronen, M., Frilander, M.J., and Thesleff, I., 2010.
452
Tooth morphogenesis and ameloblast differentiation are regulated by micro-RNAs. Dev.
453
Biol., 340, pp. 355-68.
454
455
456
457
458
459
460
McCollum, M.A., 1999. The robust australopithecine face: a morphogenetic perspective.
Science, 284, pp. 301-5.
Miller, J.A., 1991. Does brain size variability provide evidence of multiple species in Homo
habilis? Am. J. Phys. Anthropol., 84, pp. 385-98.
Miller, J.A., 2000. Craniofacial variation in Homo habilis: an analysis of the evidence for
multiple species. Am. J. Phys. Anthropol., 112, pp. 103-28.
Munne, P.M., Tummers, M., Järvinen, E., Thesleff, I., and Jernvall, J., 2009. Tinkering with
461
the inductive mesenchyme: Sostdc1 uncovers the role of dental mesenchyme in limiting
462
tooth induction. Development, 136, pp. 393-402.
463
Nanda, R.S., 1954. Agenesis of the third molar in man. Amer. J. Orthodont., 40, pp. 698-706.
464
21
465
466
Newman, T.K., Jolly, C.J., and Rogers, J., 2004. Mitochondrial phylogeny and systematics of
baboons (Papio). Am. J. Phys. Anthropol., 124, pp. 17-27.
467
Peterkova, R., Lesot, H., Viriot, L., and Peterka, M., 2005. The supernumerary cheek tooth in
468
tabby/EDA mice-a reminiscence of the premolar in mouse ancestors. Arch. Oral Biol.,
469
50, pp. 219-25.
470
471
472
473
474
475
476
Peterson, K.J., Summons, R.E., and Donoghue, P.C., 2007. Molecular palaeobiology.
Palaeontol., 50(4), pp. 775-809.
Plavcan, J.M., and Gomez, A.M., 1993. Dental scaling in the Callitrichinae. Int. J. Primatol.,
14(1), pp. 177-92.
Polly, P.D., 2007. Evolutionary biology: development with a bite. Nature, 449(7161), pp. 41315.
Polly, P.D., 2008. Developmental dynamics and G-Matrices: Can morphometric spaces be used
477
to model phenotypic evolution? J. Evolution. Biol., 35(2), pp. 83-96.
478
Raff, R., 2007. Written in stone: fossils, genes and evo-devo. Nature, 8, pp. 911-20.
479
Renaud, S., Pantalacci, S., and Auffray, J.C., 2011. Differential evolvability along lines of least
480
481
482
483
484
485
486
resistance of upper and lower molars in island house mice. PLoS ONE, 6, e18951.
Renvoise, E., Evans, A.R., Jebrane, A., et al., 2009. Evolution of mammal tooth patterns: new
insights from a developmental prediction model. Evolution, 63, pp. 1327-40.
Robinson, J.T., 1956. The dentition of the Australopithecinae. Transvaal Museum Memoir, 9,
1-179.
Rohlf, F.J., 2009. tpsDig. Version 2.14. Department of Ecology and Evolution, State University
of New York.
487
22
488
489
490
491
Salazar-Ciudad, I., and Jernvall, J., 2002. A gene network model accounting for development
and evolution of mammalian teeth. P. Natl. Acad. Sci. USA, 99, pp. 8116-20.
Salazar-Ciudad, I., and Jernvall, J., 2004. How different types of pattern formation mechanisms
affect the evolution of form and development. Evol. Dev., 6, pp. 6-16.
492
Salazar-Ciudad, I., and Jernvall, J., 2010. A computational model of teeth and the
493
developmental origins of morphological variation. Nature, 464, pp. 583-6.
494
495
496
497
498
499
500
501
502
Smith, B.H., 1994. Patterns of dental development in Homo, Australopithecus, Pan, and Gorilla.
Am. J. Phys. Anthropol., 94, pp. 307-25.
Smith, R.J., 2009. Use and misuse of the reduced major axis for line‐fitting. Am. J. Phys.
Anthropol., 140(3), pp. 476-86.
Strait, D.S., and Grine, F.E., 2004. Inferring hominoid and early hominid phylogeny using
craniodental characters: the role of fossil taxa. J. Hum. Evol., 47, pp. 399-452.
Strait, D.S., Grine, F.E., and Moniz, M., 1997. A reappraisal of early hominid phylogeny. J.
Hum. Evol., 32, pp. 17-82.
Strait, D.S., Richmond, B.G., Spencer, M.A., et al. 2007. Masticatory biomechanics and its
503
relevance to early hominid phylogeny: an examination of palatal thickness using finite-
504
element analysis. J. Hum. Evol., 52(5), pp. 585-99.
505
Suwa, G., Wood, B., and White, T.D., 1994. Further analysis of mandibular molar crown and
506
cusp areas in Pliocene and early Pleistocene hominids. Am. J. Phys. Anthropol., 93, pp.
507
407- 26.
508
509
510
Swindler, D.R., 1998. Introduction to the Primates. Seattle: University of Washington
Press.
Swindler, D.R., 2002. Primate Dentition. Cambridge: Cambridge University Press.
23
511
Tummers, M., and Thesleff, I., 2003. Root or crown: a developmental choice orchestrated by
512
the differential regulation of the epithelial stem cell niche in the tooth of two rodent
513
species. Development, 130(6), pp. 1049-57.
514
515
516
Tummers, M., and Thesleff, I., 2009. The importance of signal pathway modulation in all
aspects of tooth development. J. Exp. Zool. B, 312(4), pp. 309-19.
Vogel, E.R., van Woerden, J.T., Lucas, P.W., et al., 2008. Functional ecology and evolution
517
of hominoid molar enamel thickness: Pan troglodytes schweinfurthii and Pongo
518
pygmaeus wurmbii. J. Hum. Evol., 55(1), pp. 60-74.
519
520
521
Wilson, G.P., Evans, A.R., Corfe, I.J., et al., 2012. Adaptive radiation of multituberculate
mammals before the extinction of dinosaurs. Nature, 483(7390), pp. 457-60.
Wood, B., 1988. Are “‘robust’” australopithecines a monophyletic group? In: F.E. Grine,
522
ed. Evolutionary History of the Robust Australopithecines. New York: Aldine de
523
Gruyter, pp. 269-84.
524
Wood, B., 1992. Early hominid species and speciation. J. Hum. Evol., 22(4), pp. 351-65.
525
Wood, B., and Chamberlain, A.T., 1986. Australopithecus: grade or clade. In: B. Wood, L.
526
Martin, and P. Andrews, eds. Major Topics in Primate and Human Evolution.
527
Cambridge: Cambridge University Press, pp. 220-48.
528
529
530
531
532
Wood, B., and Chamberlain, A., 1987. The nature of affinities of the robust australopithecines.
J. Hum. Evol., 16, pp. 625-41.
Wood, B., and Collard, M., 1999a. The changing face of the genus Homo. Evol. Anthropol., 8,
pp. 195-207.
Wood, B., and Collard, M., 1999b. The human genus. Science, 284, pp. 65-71.
533
24
534
535
536
537
538
539
Wood, B., and Richmond, B., 2000. Human evolution : taxonomy and paleobiology. J. Anat.,
196, pp. 19-60.
Wood, B., and Schroer, K., 2012. Reconstructing the diet of an extinct hominin taxon: the role
of extant primate models. Int. J. Primatol., 33, pp. 716-42.
Wood, B., and Uytterschaut, H., 1987. Analysis of the dental morphology of Plio- Pleistocene
hominids. III. Mandibular premolar crowns. J. Anat., 154, pp. 121.
540
Zinner, D., Groeneveld, L.F., Keller, C., and Roos, C., 2009. Mitochondrial phylogeography of
541
baboons (Papio spp.): indication for introgressive hybridization. BMC Evol. Biol., 9, pp.
542
83.
543
9. SUPPLEMENTARY MATERIAL
544
There is no supplementary material for this manuscript.
545
10. TABLES
546
25
547
548
549
550
551
552
553
Table 1. Reduced major axis (RMA) regression results for the molar cascade (M1-M3) in extant primates
and fossil hominins. INT is the intercept, and C.I. is the 95% confidence interval. For the criterion
“Fits IC?”, values denote whether or not the sample could be described by the predictions of the
inhibitory cascade as applied to a murine sample (Kavanagh et al., 2007; Renvoise et al., 2009).
“Y” denotes yes, and “N” denotes no. Each genus sample is equally weighted by representative
species. All extant samples are equally weighted by sex.
Taxon
N
IC murine prediction
INT
C.I.
Min
C.I.
Max
-1.00
C.I.
Min
Slope
C.I.
Max
2.00
R2
C.I.
Min
C.I.
Max
Fits
IC?
1.00
Cercopithecoids
Cercocebus
C. atys
C. torquatus
Cercopithecus
C. diana
C. mitis
Colobus
C. angolensis
C. guereza
Lophocebus
L. albigena
L. johnstoni
Macaca
M. cyclopis
M. fascicularis
M. nemestrina
Papio
P. anubis
P. cynocephalus
P. ursinus
Presbytis
P. potenziani
P. rubicunda
8
4
4
24
12
12
24
12
12
16
8
8
30
10
10
10
24
8
8
8
32
16
16
-0.49
-0.14
-1.34
0.16
0.46
-0.30
-1.10
-0.66
-0.69
-2.27
-1.22
-3.51
-0.89
-2.85
-2.10
-0.21
-0.21
-1.53
-0.54
-0.06
-0.39
-1.39
-0.24
-2.78
-2.40
-14.21
-0.33
-0.05
-0.90
-2.08
-2.22
-2.00
-7.07
-5.89
-18.28
-1.53
-5.20
-5.24
-1.71
-0.61
-3.71
-2.24
-0.60
-1.07
-2.87
-1.00
0.61
2.07
7.64
0.48
0.97
3.09
4.58
5.35
3.45
-0.81
0.37
14.56
-0.26
6.96
-0.30
2.96
0.16
1.01
0.92
0.60
0.15
4.96
3.22
1.48
1.23
2.07
0.86
0.65
1.20
2.18
1.76
1.92
2.95
2.17
3.93
2.07
3.43
3.08
1.55
1.52
2.56
1.74
1.42
1.50
2.35
1.37
0.68
-0.46
-4.50
0.60
0.26
-1.44
-2.34
-2.93
-1.35
1.83
0.93
-10.54
1.56
-3.44
1.55
-1.06
1.27
0.78
0.65
1.02
1.01
-3.11
-1.91
3.10
2.80
11.33
1.26
1.04
1.69
3.01
3.07
2.98
6.82
5.91
15.74
2.56
5.10
5.70
2.67
1.82
4.37
2.86
1.80
2.09
3.65
2.07
0.42
0.64
0.19
0.30
0.29
0.25
0.07
0.06
0.22
0.39
0.34
0.11
0.52
0.20
0.56
0.24
0.78
0.56
0.45
0.88
0.26
0.03
0.02
0.09
0.04
0.03
0.03
0.02
0.00
0.00
0.00
0.00
0.08
0.05
0.00
0.31
0.00
0.06
0.00
0.56
0.04
0.01
0.70
0.11
0.00
0.00
0.91
1.00
1.00
0.58
0.65
0.76
0.47
0.62
0.86
0.69
0.91
0.64
0.73
0.71
0.91
0.69
0.90
0.96
0.92
0.99
0.50
0.48
0.27
Y
Y
Y
N
N
N
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
N
Y
Y
N
Y
Y
Y
24
12
12
24
12
12
18
16
8
8
-1.28
-0.46
-2.17
-0.61
-0.64
-0.89
-0.70
-0.66
-1.49
-0.26
-3.12
-3.31
-5.27
-1.29
-1.49
-2.31
-1.50
-1.15
-2.59
-1.57
-0.14
3.80
4.28
0.00
2.19
2.78
-0.21
0.20
0.12
2.72
2.06
1.39
2.77
1.52
1.56
1.76
1.52
1.59
2.23
1.24
1.14
-2.05
-2.48
0.98
-1.16
-1.52
1.07
0.82
0.88
-1.50
3.56
3.72
5.22
2.14
2.39
3.03
2.22
2.01
3.11
2.44
0.07
0.02
0.15
0.28
0.15
0.11
0.48
0.62
0.53
0.38
0.00
0.00
0.00
0.05
0.00
0.00
0.19
0.31
0.08
0.01
0.36
0.53
0.69
0.53
0.51
0.52
0.75
0.91
0.95
0.94
Y
Y
Y
Y
Y
Y
Y
Y
Y
Y
12
6
6
12
6
6
12
6
6
-1.12
-4.39
0.14
-0.45
-0.04
3.38
0.30
0.69
-0.57
-3.77
-6.93
-1.84
-1.13
-1.08
-29.80
-0.35
0.11
-1.56
0.15
17.32
0.52
3.43
3.02
9.63
0.69
1.51
0.52
1.90
4.37
0.85
1.46
1.09
-1.92
0.86
0.59
1.59
0.87
12.48
0.57
-2.03
-1.96
-7.12
0.59
-0.03
0.69
3.93
6.18
2.48
1.96
2.23
25.24
1.41
0.94
2.48
0.39
0.41
0.73
0.03
0.54
0.11
0.72
0.65
0.82
0.10
0.00
0.11
0.00
0.03
0.00
0.38
0.03
0.52
0.80
0.93
1.00
0.85
1.00
1.00
0.91
1.00
1.00
Y
Y
Y
N
Y
Y
N
N
Y
Hominoids
Gorilla
G. beringei
G. gorilla
Hylobates
H. agilis
H. lar
Pan troglodytes
Pongo
P. abelii
P. pygmaeus
Fossil hominins
554
Australopithecus
Au. afarensis
Au. africanus
Homo
H. erectus s.l.
H. habilis s.l.
Paranthropus
P. boisei
P. robustus
26
555
556
557
558
559
560
561
Table 2. Reduced major axis (RMA) regression results for the premolar-molar cascade (P4-M2)
in extant primates and fossil hominins. INT is the intercept, and C.I. is the 95% confidence interval.
For the criterion “Fits IC?”, values denote whether or not the sample could be described by the
predictions of the inhibitory cascade as applied to a murine sample (Kavanagh et al., 2007;
Renvoise et al., 2009). “Y” denotes yes, and “N” denotes no. Each genus sample is equally
weighted by representative species. All extant samples are equally weighted by sex.
Taxon
N
IC prediction (molar)
INT
C.I.
Min
C.I.
Max
-1.00
C.I.
Min
Slope
C.I.
Max
2.00
R2
C.I.
Min
C.I.
Max
Fits
IC?
1.00
Cercopithecoids
Cercocebus
C. atys
C. torquatus
Cercopithecus
C. diana
C. mitis
Colobus
C. angolensis
C. guereza
Lophocebus
L. albigena
L. johnstoni
Macaca
M. cyclopis
M. fascicularis
M. nemestrina
Papio
P. anubis
P. cynocephalus
P. ursinus
Presbytis
P. potenziani
P. rubicunda
8
4
4
24
12
12
24
12
12
16
8
8
30
10
10
10
24
8
8
8
32
16
16
0.26
0.86
-0.81
0.11
0.28
-0.54
0.26
0.57
0.21
-0.17
-1.15
0.00
-0.46
0.63
-0.19
-1.16
-0.69
0.38
0.28
-2.65
-0.03
0.20
-0.23
-0.14
-27.39
-7.84
-0.37
-0.43
-1.10
-0.08
-0.24
-0.46
-1.46
-10.38
-0.45
-1.13
-0.14
-0.91
-2.80
-2.08
-0.35
-1.55
-5.91
-0.50
-0.12
-1.09
0.58
4.10
0.30
0.54
3.66
0.24
0.53
2.79
0.64
0.53
1.07
0.45
0.02
1.07
0.13
4.89
0.41
1.10
1.11
8.42
0.34
0.54
0.28
1.05
0.74
2.09
1.20
1.08
1.66
1.05
0.84
1.08
1.38
2.07
1.24
1.61
0.95
1.32
2.16
1.87
1.04
1.26
3.38
1.12
0.97
1.21
0.82
-1.55
1.10
0.88
-1.63
1.07
0.85
-0.68
0.75
0.92
0.56
0.93
1.27
0.62
1.07
-2.90
1.15
0.62
0.78
-4.57
0.89
0.80
0.86
1.35
20.00
8.00
1.54
1.65
2.03
1.32
1.44
1.59
2.25
8.06
1.55
2.11
1.55
1.77
3.50
2.83
1.50
2.53
5.63
1.43
1.25
1.78
0.67
0.41
0.98
0.48
0.25
0.72
0.67
0.28
0.79
0.51
0.26
0.85
0.43
0.72
0.83
0.08
0.15
0.57
0.61
0.00
0.42
0.83
0.53
0.29
0.00
0.84
0.12
0.00
0.13
0.29
0.02
0.40
0.21
0.06
0.43
0.20
0.19
0.43
0.00
0.00
0.10
0.22
0.00
0.18
0.58
0.20
0.86
1.00
1.00
0.75
0.72
0.94
0.87
0.71
0.96
0.89
0.75
0.99
0.69
0.94
0.98
0.65
0.44
0.90
0.90
0.63
0.65
0.94
0.78
N
Y
Y
N
N
Y
N
N
N
N
Y
N
Y
N
N
Y
Y
N
Y
Y
N
N
N
24
12
12
24
12
12
18
16
8
8
-0.10
-0.17
-0.02
0.22
-0.57
-0.89
0.56
-0.10
0.74
0.27
-0.46
-0.79
-0.55
-0.20
-1.64
-2.36
0.22
-0.54
0.40
-0.71
0.24
0.30
0.59
0.54
3.57
2.62
1.04
2.84
1.68
0.70
1.29
1.34
1.24
0.92
1.36
1.76
0.77
1.23
0.63
0.86
1.07
1.01
0.82
0.70
-1.11
-1.34
0.47
-1.13
-0.13
0.52
1.55
1.74
1.58
1.18
1.96
3.09
1.01
1.54
0.88
1.63
0.63
0.56
0.64
0.59
0.28
0.11
0.36
0.24
0.60
0.65
0.32
0.13
0.14
0.36
0.01
0.00
0.03
0.00
0.02
0.23
0.86
0.93
0.89
0.80
0.70
0.49
0.67
0.63
0.97
0.95
N
N
N
N
N
Y
N
N
N
N
14
7
7
10
5
5
14
7
7
0.13
0.59
-0.91
-0.90
-0.27
-7.01
0.31
3.09
0.09
3.09
-1.25
0.17
-5.63
-4.77
-1.93
-16.57
-0.33
-1.25
-1.08
-1.25
2.45
1.13
6.20
7.27
3.23
14.76
0.85
4.11
0.69
4.11
1.21
0.93
1.84
1.57
1.11
5.37
0.98
-1.42
1.10
-1.42
-0.40
0.56
-2.55
-3.25
-0.89
-7.50
0.63
-2.26
0.74
-2.26
2.18
1.18
4.94
3.94
1.93
11.08
1.46
2.51
1.96
2.51
0.26
0.80
0.02
0.06
0.60
0.23
0.50
0.01
0.77
0.01
0.01
0.08
0.00
0.00
0.04
0.01
0.01
0.00
0.15
0.00
0.79
1.00
0.97
0.57
1.00
1.00
0.84
0.69
1.00
0.69
Y
N
Y
Y
N
Y
N
Y
N
Y
Hominoids
Gorilla
G. beringei
G. gorilla
Hylobates
H. agilis
H. lar
Pan troglodytes
Pongo
P. abelii
P. pygmaeus
Fossil hominins
Australopithecus
Au. afarensis
Au. africanus
Homo
H. erectus s.l.
H. habilis s.l.
Paranthropus
P. boisei
P. robustus
27
562
11. FIGURE LEGENDS
563
Figure 1. The inhibitory cascade is presented as a dashed line plotting the function y = 1 + [(a –
564
i)/i](x – 1), which describes how the rates of activation and inhibition affect molars as they
565
develop in sequence. M2:M1 and M3:M1 are ratios of relative molar size. As the ratio of M2:M1
566
ratio increases, the ratio of M3:M1 also increases, showing a high degree of activation acting
567
along the molar row. The opposite, a decrease in molar ratios, denotes high rates of inhibition.
568
Gray shading indicates areas of general size reduction or increase in the postcanine tooth row
569
and is bounded by cases where M1=M2 and M1=M3.
570
Figure 2. Regression of the relative occlusal areas of the molars of extant primates, faceted by
571
genus. The line represents the function of the inhibitory cascade. Gray solid circles =
572
cercopithecoids; black solid diamonds = hominoids.
573
Figure 3. Regression of the relative occlusal areas of the molars of fossil hominins and extant
574
primates. The solid line represents the function of the inhibitory cascade and the dashed line is a
575
least squares regression of the extant specimens. Solid symbols = extant taxa; unfilled symbols =
576
fossil hominins. Gray solid circles = cercopithecoids; black solid diamonds = hominoids.
577
Unfilled squares = Australopithecus; unfilled circles = Homo, unfill upward triangles =
578
Paranthropus boisei and unfilled downward triangles = Paranthropus robustus.
579
Figure 4. Regression of the relative occlusal areas of the molars of fossil hominins, faceted by
580
taxon. The solid line represents the function of the inhibitory cascade, and the dashed line is a
581
least squares regression of the extant specimens. Unfilled squares = Australopithecus; unfilled
582
circles = Homo, unfilled upward triangles = Paranthropus boisei and unfilled downward
583
triangles = Paranthropus robustus. Specimens which deviate notably from the inhibitory cascade
584
are labeled.
28
585
Figure 5. Regression of the relative occlusal areas of the last premolar and first two molars of
586
extant primates, faceted by genus. The line represents the function of the inhibitory cascade.
587
Gray solid circles = cercopithecoids; black solid diamonds = hominoids.
588
Figure 6. Regression of the relative occlusal areas of the last premolar and first two molars of
589
fossil hominins and extant primates. The line represents the function of the inhibitory cascade.
590
Solid symbols = extant taxa; unfilled symbols = fossil hominins. Gray solid circles =
591
cercopithecoids; black solid diamonds = hominoids. Unfilled squares = Australopithecus;
592
unfilled circles = Homo, unfilled upward triangles = Paranthropus boisei and unfilled downward
593
triangles = Paranthropus robustus.
594
Figure 7. Regression of the relative occlusal areas of the last premolar and first two molars of
595
fossil hominins, faceted by taxon. The line represents the function of the inhibitory cascade.
596
Solid symbols = extant taxa; unfilled symbols = fossil hominins. Gray solid circles =
597
cercopithecoids; black solid diamonds = hominoids. Unfilled squares = Australopithecus;
598
unfilled circles = Homo, unfilled upward triangles = Paranthropus boisei and unfilled downward
599
triangles = Paranthropus robustus.
29
Download