interspecific scaling and ontogenetic growth

Interspecific Scaling and Ontogenetic Growth Patterns of the Skull in Living and Fossil Ctenomyid and Octodontid rodents (Caviomorpha: Octodontoidea) Efecto del tamaño entre especies y patrón de crecimiento ontogenético del cráneo en roedores ctenómidos y octodóntidos (Caviomorpha: Octodontoidea) Aldo I. Vassallo and Matías S. Mora Dedication This work is dedicated to the memory of Oliver Paynie Pearson for his great contributions to increase our knowledge of North and South American mammals and his efforts to help the careers of his colleagues, especially young South American biologists. ABSTRACT We assessed the effect of size on skull attributes of ctenomyid and octodontid rodent species using an allometric approach. We focus on traits which have long been considered of relevance for tooth digging, such as the development of the mandibular angle and masseteric crest, and the robustness of incisors. Interspecific comparisons of adult specimens revealed important shape differences between Ctenomys, on one hand, and octodontid genera (except Spalacopus and, partly, Aconaemys) plus the early ctenomyid Actenomys, on the other. In addition, we found that larger Ctenomys species possess both proportionally broader lower jaws and more robust incisors. For these traits, the ontogenetic trajectories of the skull in the small Ctenomys talarum and large C. australis do not differ in either slope (allometric coefficient) or intercept. In this sense, our study clearly shows that evolutionary ontogenetic scaling was associated with skull shape variation within the limits of a single genus, Ctenomys. On the other hand, C. australis and the extinct Actenomys, which differ sharply in skull morphology and possibly in fossorial habits and ecological niche, differ significantly in the slope and/or intercept of their ontogenetic trajectories. This fact indicates the complexity of changes in development responsible for the departure from ontogenetic scaling in ancient and extant ctenomyines, in association with morphological diversification of the skull above the species level. Key words: allometry, Ctenomys, ontogeny, Rodentia, skull

University of California Publications in Zoology

RESUMEN Se utilizó una aproximación alométrica para analizar el efcto del tamaño sobre caracteres craneanos en roedores octodóntidos y ctenómidos. Se enfatizó en aquellos caracteres considerados como adaptaciones a la excavación con los incisivos, tales como el desarrollo del ángulo mandibular, la cresta masetérica y la robustez de los incisivos. Las comparaciones interespecíficas, realizadas en base a especímenes adultos, revelaron importantes diferencias en la forma craneana entre Ctenomys, por un lado, y géneros octodóntidos (excepto Spalacopus y, parcialmente, Aconaemys) más el ctenomino extinto Actenomys, por el otro. Además, las especies de Ctenomys de mayor tamaño mostraron mandíbulas proporcionalmente más anchas e incisivos más robustos en sección transversal. Para estos caracteres, las trayectorias ontogenéticas del cráneo en la especie de pequeño tamaño Ctenomys talarum y en la de mayor tamaño C. australis no difirieron ni en la pendiente (coeficiente de alometría) ni en la intersección. En este sentido, el presente análisis muestra claramente que un crecimiento ontogenético evolutivo se asocia con la variación en la forma del cráneo dentro de los límites de un género, Ctenomys. En forma contrastante, C. australis y el extinto Actenomys, que difieren marcadamente en la morfología del cráneo y, posiblemente, en sus hábitos excavadores y nicho ecológico, difieren significativamente en la pendiente y/o en la intersección, de sus trayectorias ontogenéticas. Este hecho indica que, al comparar ctenominos primitivos y actuales, cambios complejos en el desarrollo produjeron un apartamiento del simple crecimiento ontogenético, en asociación con una diversificación morfológica del cráneo por sobre el nivel de especie. Palabras clave: alometría, Ctenomys, ontogenia, Rodentia, cráneo INTRODUCTION Morphological adaptation usually produces changes in the relative proportions of body parts, resulting in enhanced functional performance relative to particular locomotor or feeding habits. The allometric approach, which deals with variation in particular body parts associated with variation of the overall size of organisms, has been a useful way to study adaptation in living and fossil lineages (Emerson and Bramble, 1993; Silva, 1998). Allometric relationships generally are interpreted as reflecting changes in physiological and structural requirements associated with changes in body size (Schmidt-Nielsen, 1991). It has been proposed that particular functional requirements associated, for example, with particular locomotor habits or behaviors exert selective pressures changing the “normal” proportions among body parts (Fairbairn, 1992). For example, a study of interspecific allometry of limb proportions in digging ctenomyid rodents (Casinos et al., 1993) showed that a particular locomotor activity can exert selective pressure on long bone design; by analyzing the diameter/length relationship, they showed that for a given diameter the corresponding length was relatively low. The position of fossil taxa in relation to the regression line calculated from living species allowed the authors to suggest a “morphocline,” the plesiomorphic state of which would be represented by the fossil taxon, with long bone design similar to that of generalized, surface dwelling rodents (Figs. 1-4 in Casinos et al., 1993). Rodent skulls exhibit some of the most specialized sets of traits associated with

Vassallo and Mora: Scaling in Living and Fossil Octodontoid Rodents

processing hard vegetal foods (Hanken and Hall, 1993; Satoh, 1997; Feldhamer et al., 1999). This includes extremely variable occlusal patterns of the cheek teeth, highly developed masseteric and pterygoid musculature (which acts within an advantageous mechanical context), and ever-growing upper and lower incisors, shared with the lagomorphs and some unrelated fossil taxa (example Paedotherium, Notoungulata) (Maynard-Smith and Savage, 1959; Woods, 1972; Butler, 1985; Wake, 1993; Koenigswald et al., 1994; Neveu and Gasc, 1999). Rodent incisors may represent exaptations for a broad array of non-feeding functions and behaviors, such as dam construction in beavers, colony defense in bathyergids, and tunnel excavation in several rodent groups. Besides the well-known positive allometry between rostral length and basicranium length for mammals in general (Radinsky, 1985), Vassallo (2000) recently showed a nearly isometric relationship between out-lever and in-lever arms of the masseteric musculature in caviomorph rodents, and hence the maintenance of a given mechanical relationship, in spite of substantial variation in size. The sister taxa Ctenomyidae and Octodontidae (Rodentia: Caviomorpha) includes 8 living genera which have evolved a number of morphological, physiological, and behavioral adaptation to fossorial and subterranean habits (Pearson, 1959; Mares and Ojeda, 1982; Reig, 1986; Kohler et al., 2000; Gallardo and Kirsch, 2001; Olivares et al., 2004). Seven of these genera are grouped within the family Octodontidae, representing a diverse array of specializations to fossorial habits, from surface dwelling forms such as Octodontomys gliroides, to fully subterranean species such as Spalacopus cyanus (Reig, 1970; Pearson, 1984; Begall and Gallardo, 2000). In contrast, the remaining genus (Ctenomys, family Ctenomyidae) includes about 60 extant fully subterranean species (Reig, 1986; Reig et al., 1990; Lessa and Cook, 1998; Lacey et al., 2000). In addition, various ctenomyid fossil taxa add to the morphological diversity of the family (Reig and Quintana, 1992; Fernández et al., 2000; Verzi, 2002). The lateral expansion of the angular process and masseteric crest of the mandible, which are indicators of masseter development, and a greater cross sectional area of the incisors are two traits considered to be key adaptations for tooth digging in subterranean ctenomyids (Verzi, 1994, 2002; Fernandez et al., 2000; Mora et al., 2003). A strong masseteric musculature produces great in-forces which, in turn, result in out-forces at the tip of incisors sufficient for breaking hard soils (Hildebrand, 1985; Lessa, 1990; Vassallo, 1998; Stein, 2000). On the other hand, the cross sectional area of the incisors is correlated with resistance to shearing and bending stress, which is of importance in particular feeding habits and digging behaviors (Biknevicius et al, 1996; Bacigalupe et al, 2002; Mora et al; 2003). Interspecific morphological analysis and allometric studies on adult specimens (Verzi, 1994, 2002; Fernández et al., 2000; Mora 2001; Olivares, 2001; Mora et al., 2003) has demonstrated considerable variation in skull shape among living and early ctenomyids. However, no studies have integrated neontological variation in skull shape among taxa to evolutionary changes in the ontogeny. The integration of these 2 data sets is crucial to our understanding of morphological evolution within the highly diverse Octodontidae and Ctenomyidae. Here, we analyze interspecific scaling, and postnatal intraspecific growth pattern of skull traits having important functional and ecological correlates, such as the angular process of the mandible and the cross sectional area of the incisors, to assess possible ontogenetic changes underlying the shape differences present among living and fossil taxa. Specifically, we investigate the evolution of ontogenetic trajectories at 2 different hierarchical levels: interspecific variation among extant species within the genus Ctenomys, and inter-generic variation


between this genus and the ancestral ctenomyine Actenomys. Material and Methods Interspecific Scaling Relations The analysis presented here was based on skulls of 164 adult specimens of 21 species of Ctenomys (C. argentinus, C. australis, C. azarae, C. boliviensis, C. bonettoi, C. dorbignyi, C. haigi, C. latro, C. leucodon, C. magellanicus, C. mendocinus, C. occultus, C. opimus, C. perrensi, C. porteousi, C. pundti, C. rionegrensis, C. roigi, C. talarum, C. tuconax, C. tucumanus); 15 adult specimens of Octodon (7 O. bridgesi and 8 O. degus); 7 adult specimens of Spalacopus cyanus; 2 adult specimens of Aconaemys sagei; and 6 adult specimens of Octodontomys gliroides. Five well-preserved adult specimens of the Pliocene genus Actenomys were also included. The following linear measurements were taken using a digital caliper (to the nearest 0.01 mm): upper incisor width and thickness; mandibular width across the masseteric crests; basicranium axis length (see Fig. 1 in Mora et al., 2003). Incisor cross section, as a measure of resistance to shearing and bending stress, was calculated according to Biknevicius et al. (1996). The basicranium axis length (length of basioccipital plus basisphenoid) was used as a conservative measure of size that changes little when other skull characters do change markedly (Radinsky, 1985). A detailed list of specimens and localities is provided in the appendix. Ontogenetic Sequences of Ctenomys The analysis of ontogenetic growth pattern was based on skulls of 16 adults and 38 juvenile and subadult specimens (Ctenomys australis) and 22 adults and 49 juvenile and subadult specimens (Ctenomys talarum) (see “Specimens Examined”). Individuals were collected at Necochea, Buenos Aires Province, Argentina, during ecological censuses, mainly in 1987-1988. We recorded the upper incisor width and thickness, mandibular width across the masseteric crests, condylo-incisor length (i.e., the distance between the jaw condyle and the tip of the lower incisor, as a measure of out-lever arm of jaw adductor muscles), mandibular height at the level of m1, and basicranium axis length using a digital caliper (to the nearest 0.01 mm). In spite of significant sexual body size dimorphism (Malizia et al., 1991) no significant differences were detected between the growth curves of males and females (neither the allometric coefficient nor the y-intercept) when these skull traits were “standardized” against size (basicranium length); consequently, we pooled sexes in subsequent analysis. Ontogenetic Sequences of Actenomys Analyses were based on 21 lower jaws ranging from small, presumably newborn individuals, to adult specimens. Individuals came from the collection of Museo de Ciencias Naturales “Lorenzo Scaglia”, Mar del Plata, Argentina (see appendix). The following measurements were taken using a digital caliper (to the nearest 0.01 mm): condylo-incisor length, lower incisor width and thickness, mandibular width across the masseteric crests. In most cases, mandibles were the only fragment present or the skull was partially or totally destroyed. Hence, we used mandibular height at the level


of m1 as a measure of size increase during ontogeny (instead of basicranium length); this should serve as a good proxy for size, as basicranium length and mandibular height in Ctenomys australis are significantly correlated (r = 0.81, t = 6.70, p < 0.001). Allometric Analyses For the purpose of both interspecific and ontogenetic analyses, linear cranial measurements were log10 transformed. Bivariate equations were calculated as reduced major axis Model II regressions because neither variable is considered independent (i.e., there was error associated with the measurements of both x and y) and it is the structural relationship between the 2 variables that is required. The slope, the intercept, and their respective confidence intervals were calculated according to the computation method provided by Legendre and Legendre (1998; see also Sokal and Rohlf, 1981). Because of the high correlation between the skull variables analyzed and basicranium axis length, similar results were obtained with Model I (least squares) regression. We tested slopes and elevation with analysis of covariance (ANCOVA; Zar, 1984). For our analysis of interspecific scaling relations the traditional allometric approach fails to account for non-independence of taxa (Harvey and Pagel, 1991), so we also analyzed the skull measurements using phylogenetically independent contrasts (Felsenstein, 1985). Log10 data were converted to phylogenetically independent standardized contrasts using the PDTREE module of the phylogenetic diversity program (PDAP) version 5.0 (Garland et al., 1993). Standardization tests in PDTREE indicated that Grafen’s branch length transformation (Grafen, 1992) was the appropriate method for assigning arbitrary branch lengths (Garland et al., 1992). This method assumes a gradual Brownian motion model of evolution, and the height of each node is proportional to the number of species derived from it. Slopes, confidence intervals, and other regression statistics were obtained from PDTREE. No complete phylogeny of Ctenomys species exists, so we combined partial phylogenies of Cook and Lessa (1998), Lessa and Cook (1998), and Ortells and Barrantes (1994), all based on molecular evidence, to obtain the phylogenetic tree used in PDTREE. RESULTS Interspecific Scaling Across 21 species of Ctenomys, the fossil ctenomyid Actenomys, and 5 species of octodontid rodents, both mandibular width and incisor cross section were significantly and positively associated with basicranium length (Fig. 1). In Ctenomys, the mandibular width across the masseteric crest, as a measure of masseter development, increases with positive allometry (allometric coefficient = 1.28 [95% C.I.: 1.22-1.36]) with respect to basicranium length (Table 1; Fig. 1A). Larger Ctenomys species thus possess proportionally broader lower jaws. Results obtained by the method of phylogenetically independent contrasts for continuous variables did not differ from those obtained by traditional reduced major axis regression (allometric coefficient = 1.30 [95% C.I.: 1.041.56], N = 20 contrasts; Fig. 2A), although the 95% confidence interval was broader for independent contrasts. The analysis of the effect of size on skull allometry was precluded in the Octodontidae because the genera within this taxa show limited


1,8

log10 mandibular width

1,7 1,6 1,5 1,4 1,3 1,2

1

1,1

1,2

1,3

1,4

log10 basicranium length

log10 incisor cross section0.5

1,4 1,2 1 0,8 0,6 0,4 0,2

1

1,1

1,2

1,3

1,4

log10 basicranium length

Figure 1. Graph of logarithmic coordinates of skull measurements in octodontoid rodents. Solid squares, Ctenomys; open squares, Aconaemys sagei; solid triangles, Octodontomys gliroides; open triangles, genus Octodon; open circles, Spalacopus cyanus; solid circles, Pliocene fossile ctenomyine Actenomys. A: mandibula width vs. basicranium length; B: incisor cross section vs. basicranium length. Regression lin fitted only for Ctenomys.


Table 1.- Allometric equations (y=axb; Model II regression) of skull variables calculated for adult specimens of 21 Ctenomys species differing in body size (see Methods and “Specimens Examined”), and ontogenies of C. australis, C. talarum and the early Pliocene ctenomyine Actenomys. Abbreviations: BAS=basicranium axis length; HMC=height of the mandibular corpus at the level of m1. All variables are log10 transformed. 95% Confidence intervals

Regression Equation

r

b

a

BAS/mandibular width

y= 0.18x1.28

0.88

1.22 – 1.36

0.07 – 0.30

BAS/incisor cross section0.5

y= -1.55x1.26

0.83

1.17 – 1.36

-1.41– -1.69


y= -0.37x1.74

0.88

1.61 –1.88

-0.66 – -0.09


y= -0.97x1.32

0.95

1.25 – 1.39

-1.10 – -0.83


y= -0.41x1.61

0.97

1.55 – 1.66

-0.52 – -0.31


y= -0.85x1.20

0.98

1.16 – 1.23

-0.92 – -0.80

HMC/mandibular width

y= 0.37x1.20

0.87

0.99 – 1.45

0.06 – 0.69

HMC/incisor cross section0.5

y= -0.71x0.99

0.93

0.87 – 1.14

-0.91– -0.52

HMC/condyle-incisor length

y= 0.59x1.03

0.96

0.88 – 1.09

0.44 – 0.75

HMC/mandibular width

y= 0.38x1.15

0.98

1.00 – 1.25

0.29 – 0.47

HMC/incisor cross section0.5

y= -1.29x1.58

0.98

1.49 – 1.68

-1.42 – -1.17

HMC/condyle-incisor length

y= 0.29x1.17

0.97

1.09 – 1.26

0.19 – 0.40

Ctenomys adults

C. australis ontogeny

C. talarum ontogeny

Actenomys ontogeny

C. australis ontogeny

variation in overall size. However, it is clear that, with the exception of the subterranean Spalacopus, octodontine species fall below the trend for Ctenomys species (Fig. 1A). This is also the case for the Pliocene genus Actenomys. Under the hypothesis of geometric similarity (Schmidt-Nielsen, 1991), the log10 square root of incisor cross section must scale to log10 basicranium axis length with an exponent of 1 (i.e., isometry). We found a positive allometric pattern for this relationship (allometric coefficient = 1.26 [95% C.I.: 1.17-1.36]), suggesting that larger Ctenomys species have proportionally more robust incisors (Table 1; Fig 1B; Fig. 3). Results obtained by the method of phylogenetically independent contrasts for continuous variables yielded a similar allometric pattern, although the allometric coefficient was


Figure 2. Relationships of the standardized contrasts of mandibular width (A) and incisor cross section (B) vs. basicranium length in species of Ctenomys differing in body size. greater than that obtained by reduced major axis regression (allometric coefficient = 1.37 [95% C.I.: 1.18-1.57]) , number of contrasts = 20; Fig. 2B). Once again, octodontine taxa (except Spalacopus and Aconaemys) and Actenomys fall below the regression line for Ctenomys (Fig. 1B). Ontogenetic Scaling Across the ontogenetic sequences of Ctenomys talarum and C. australis, both mandibular width and incisor cross section were significantly and positively associated with basicranium axis length. For both species, mandibular width grows allometrically (Table 1; Fig. 4A; Fig. 5) reflecting the development, and strengthening, of the jaw and masseteric musculature during ontogeny. The cross sectional area of incisors also


Figure 3. X-ray lateral view of the skull of Ctenomys bonettoi (above’ body weight 100 g) and C. tucumanus (belw; body weight 240 g) showing interspecific differences in incisor robustness due to positive allometry of incisor cross section vs. skull size. Scale bar = 2 cm. grows allometrically in both species (Table 1; Fig. 4B), also reflecting the strengthening of incisors to manage bending and shearing stresses. For these 2 traits, the allometric coefficients were slightly greater in the larger C. australis. Nonetheless, the confidence intervals for both the slope and y-intercept overlap broadly between the species. An ANCOVA revealed no significant differences between the slopes (F = 2.17, d.f. = 121, p > 0.1; F = 1.08, d.f. = 121, p > 0.25; incisor cross section and mandibular width, respectively) or elevations (F = 0.26, d.f. =122, p > 0.25; F = 1.14, d.f. = 122, p > 0.25; incisor cross section and mandibular width, respectively) of C. talarum and C. australis growth curves. For the skull traits we studied, the ontogenetic pattern of growth of the extant Ctenomys australis and the Pliocene ctenomyine Actenomys (estimated mass 1300 g.; Fernández et al., 2000) differs largely, reflecting evolutionary changes in their ontogenetic trajectories (Fig. 6). The height of the mandibular corpus at the level of m1 was used as an indicator of overall size increase because the basicranium was

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Figure 4. Graph of logarithmic coordinates of skull measurements in ontogenies of 2 Ctenomys species differing in body size. Open squares, solid line: Ctenomys talarum; adult body weight 150 g; solid squares, broken line: C. australis; adult body weight 400 g. A: mandibular width vs. basicranium length; B: incisor cross section vs. basicranium length. absent or partly destroyed in most fossil specimens. For the skull trait mandibular width across the masseteric crest, the allometric coefficient calculated for Actenomys was slightly greater than that of Ctenomys (Table 1). The values of Actenomys fall below those measured in the living species (Fig. 6A). While the ANCOVA revealed


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Figure 5. Anterior view of the skull of juvenile (A; C) and adult (B; D) males of Ctenomys talarum (above) and C. australis (below) showing differences in mandibular width due to allometric growth during ontogeny. Note differences in the development of the mandibular anglle and masseteric crest between juvenile and adult specimens. Scale bar = 1 cm. no significant differences between the slopes (F = 0.46, d.f. = 50, p > 0.25), there were significant differences between the elevations (F = 15.38, d.f. = 51, p < 0.001) of the growth curves for C. australis and Actenomys. The condylo-incisor length is a measure of the out-lever arm for the adductor jaw muscles. Contrary to the pattern observed for the mandibular width, the values for C. australis here fall below those measured in Actenomys, denoting an overall shortening of the jaw in the living ctenomyine (Fig. 6B; Fig. 7), which is also indicated by the non overlapping confidence intervals of the y-intercept (Table 1), and significant differences between elevations (F = 17.50, d.f. = 51, p < 0.001; ANCOVA) of their growth curves. Inter-generic differences in incisor robustness between the extant Ctenomys australis and the Pliocene Actenomys were the outcome of a postnatal change in the direction of the ontogenetic trajectory. We found a significant difference in the allometric coefficient (Table 1) and slopes (F = 31.3, d.f. = 50, p < 0.001, ANCOVA) when comparing the growth curves relating the cross sectional area of the lower incisors vs. the height of the mandibular corpus in C. australis and the fossil ctenomyine (Fig. 6C).

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Figure 7. Lateral view of the lower jaw of the extant Ctenomys australis (above) and the Pliocene ctenomyine Actenomys (below). Note the overall shortening, particularly the condyloincisor distance, and strengthening of the jaw of C. australis. Differences in incisor thickness can also be noted. Scale bar = 1 cm.

Figure 6. Graph of logarithmic coordinates of skull measurements in ontogenies of the extant Ctenomys australis (solid squares) and the fossil ctenomyine Actenomys (open circles. A: mandibular width vs. mandibular height; B: condylo-incisor length vs. mandibular height; C: incisor cross section vs. mandibular height.


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DISCUSSION The intensification of the hystricognath condition – lateral expansion of the mandibular angle and masseteric crest (Woods, 1985) – clearly differentiates representatives of Ctenomys from genera within Octodontidae, except Spalacopus and Aconaemys (Fig. 1A; see also Vassallo and Verzi, 2001). The enlargement of the mandibular angle is related with the hypertrophy of the masseteric adductor muscles, a conjecture supported by the fact that muscle growth has a heritable epigenetic impact on bone development (Herring and Lakars, 1981). This derived condition also produces a clear difference between Ctenomys and early, fossil ctenomyids such as Actenomys, with the notable exception of Eucelophorus (see Reig and Quintana, 1992; Verzi, 2002). In conjunction with other traits, the morphological evolution of the masticatory apparatus accompanied the adaptive diversification of the families Ctenomyidae and Octodontidae, producing an array of fossil and living taxa, from surface-dwelling to very specialized, scratch and chisel-tooth digging subterranean forms. The hypertrophy of adductor muscles, mandibular angle, and the masseteric crest has been functionally related to the development of greater out-forces at the tip of the incisors, forces that are required to effectively break the soil and cut fibrous roots during digging activities and tunnel construction (Vassallo, 1998; Olivares et al., 2004). A plesiomorphic character state – characterized by a poorly developed mandibular angle and masseteric crest – independently changed to the aforementioned derived condition several times during the diversification of ctenomyid and octodontid rodents. Thus, unrelated taxa such as Ctenomys, Eucelophorus, and Spalacopus converged to a similar condition, in association with the recurrent emergence of fully subterranean habits (Lessa et al., 2004). Ctenomys show considerable variation in body size: the various species range from 90 g (C. pundti) to 700-900 g (C. tuconax, C. conoveri). Previous analysis showed that larger Ctenomys species have proportionally larger masseteric muscles, as indicated by both myological (Vassallo, 1998) and osteological data (Mora et al., 2003). The mean multivariate allometric coefficient for mandibular width with respect to a series of skull measurements used in a recent morphometric analysis was 1.13 (Mora et al., 2003). In that study we proposed that allometry could be partly responsible for altering skull proportions of extant Ctenomys species through scaling (Alberch et al., 1979; Lessa and Patton, 1989; Klingenberg, 1998). The present comparative analysis of the ontogenetic growth pattern of 2 species markedly differing in body size, C. australis and C. talarum, allowed us to draw some conclusions about this issue. The expected strong positive allometry of mandibular width vs. basicranium axis length is indicative of normal bone and muscle development, and correlated shape change during the ontogeny of Ctenomys (Fig. 4 and 5; for another example, see Abdala et al., 2001). Accordingly, the masseteric musculature represents 0.035 % (N = 5) of the body mass of young specimens of C. australis, while this figure is approximately 0.073 % (N = 8) in adult specimens (Vassallo, unpublished data). For mandibular width vs. basicranium axis length we did not find substantial differences in either the slope or the y-intercept between the ontogenies of C. talarum and C. australis (Table 1; Fig. 4A). The allometric coefficient for incisor cross section vs. basicranium length was only marginally greater in C. australis; there was no significant difference in the y-intercept between these species (Table 1; Fig. 4B). Hence, we conclude that maintenance of a given ontogenetic trajectory through the range of sizes of extant Ctenomys species (i.e., ontogenetic scaling), likely is sufficient to explain the observed shape differences between small and large species.

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Although some studies have associated ontogenetic scaling with heterochronic changes (progenesis and hypermorphosis), other changes in growth dynamics can produce the same allometric pattern; thus, inferring heterochrony from allometric data should be taken with caution (Klingenberg, 1998, and references therein). A similar pattern was observed in the North American subterranean species Thomomys townsendii (Rodentia, Geomyidae), whose increased incisor procumbency, a condition considered an adaptation for tooth digging, is solely the outcome of increased overall skull size, i.e. ontogenetic scaling (Lessa and Patton, 1989). Actenomys was an early Pliocene ctenomyid whose paleo-caves protrude on shore cliffs in southern Mar del Plata, Argentina. We chose this genus because, for several traits usually considered to be adaptations for digging in the family Ctenomyidae, it shows a plesiomorphic condition, in particular regarding the width of the jaw across the masseteric crest and the robustness of the incisors (Fig. 1; see also Verzi, 1994, 2002). In Actenomys, the long bones of both fore- and hind limbs are rather elongated, showing a slight departure from the condition seen in Octodon, indicating that aboveground locomotion was both common and agile in the fossil ctenomyid. However, Actenomys possess an incipient development of the teres major process, which could be reasonably interpreted as an indicator of daily digging activities associated with a semi-subterranean mode of life (Fernández et al. 2000; see also Schleich and Vassallo, 2003). When studying mandibular width, we found no substantial difference between the slopes of the growth curves of Actenomys and the extant subterranean species C. australis (Table 1). The values of Actenomys fall below those measured in the living species throughout the ontogenetic sequence; i.e., growth-independent shape differences exists (Fig. 6A). This parallel shift of the entire ontogenetic trajectory, termed lateral transposition (sensu Klinberger, 1998) indicates that alterations in development have occurred in early, prenatal stages. As noted above, a wider mandible results from the lateral expansion of the mandibular angle and masseteric crest and thus this trait may be used to assess muscle development in living and fossil octodontid taxa (Verzi, 1994, 2002; Vassallo and Verzi, 2001; Olivares et al., 2004). It is clear that muscle growth during the postnatal period, as reflected by the allometric relationship between mandibular width and height of the mandibular corpus for both Actenomys and Ctenomys (Table 1; Fig. 6A), results from an increase in individual muscle fiber size, or hypertrophy; the number of myofibrils within the enlarged muscle fiber can increase more than 10-fold during development (Wolpert, 1998). Thus, early embryonic, prenatal differences in the number of muscle precursor cells, myoblasts (Carlson, 1988; Langeland and Kimmel, 1997), is compatible with the lateral transposition observed between the ontogenetic trajectories of Actenomys and Ctenomys australis (Fig 6A). The overall shortening of the condylo-incisor distance during the entire postnatal ontogeny of living Ctenomys, as compared with Actenomys (Figs. 6B, 7), may lead to greater out-forces at the tip of the incisors due to the reduction of the out-lever arm of the masseters (Hildebrand, 1988; Lessa, 1990). The differences between the growth curves of these 2 taxa (i.e., lateral transposition; Fig. 6B) might be caused by prenatal differences in the overall shape of the mesenchymal condensation of neural-crestderived cells from which later originate the mandibular ramus and processes (Atchley and Hall, 1991; Wolpert, 1998). Differences in incisor robustness between extant Ctenomys species and Actenomys (Fig. 1B) resulted from a change in slope of the ontogenetic trajectory (Table 1; Fig. 6C). This evolutionary change in the direction of the ontogenetic trajectory suggests a


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possible dissociation of growth dynamics between incisor cross section and mandibular height during the postnatal sequence of C. australis and Actenomys. Rodent incisors are regenerative tissues that grow continuously throughout life. Several genetic and epigenetic factors affect mammalian tooth morphogenesis, in particular rodent incisor development (Gilbert, 1997; Harada et al., 2002). A change in the amount and/ or rate of dentin deposition, possibly associated with developmental units affecting the initial odontoblast cell population (Atchley and Hall, 1991), may be a likely factor producing the observed differences in the postnatal growth curves of fossil and extant ctenomyines. CONCLUSIONS All extant Ctenomys species are very similar in their general adaptations to life underground, particularly morphological digging adaptations of the skull and forelimbs. It seems apparent that the most variable attribute in this genus is overall body size, although all living species have similar strict subterranean habits and high digging capabilities. We found that larger Ctenomys species possess both proportionally broader lower jaws and more robust incisors. Nonetheless, for these traits, the ontogenetic trajectories of the skull in the small Ctenomys talarum and large C. australis do not differ in either slope (allometric coefficient) or intercept, in association with the conservation of the bauplan, or basic structure, of the skull. In this sense, our study strongly supports an association between evolutionary ontogenetic scaling and skull shape variation within the limits of a single genus, Ctenomys. On the other hand, C. australis and the extinct Actenomys, which sharply differ in skull morphology (Verzi, 2002; Fig. 1) and, possibly, in fossorial habits and ecological niche (Fernández et al., 2000) significantly differ in the slope and/or intercept of their ontogenetic trajectories, as demonstrated by our present analysis. This fact indicates the complexity of evolutionary changes in development responsible for the departure from ontogenetic scaling in ancient and extant ctenomyines, in association with morphological diversification of the skull above the species level. Differences between fossil and living ctenomyids, with strong adaptive implications regarding the evolution of fossorial habits, such as the strengthening of the masticatory apparatus, surely have a developmental basis, as suggested by the postnatal growth patterns presented here. It would be informative to study ontogenetic series, including prenatal stages, of some living octodontid species, such as Octodon degus, which share with the fossil Actenomys some plesiomorphic character states, like the relatively poorly developed masseteric muscles, mandibular angle, and incisor cross section. Acknowledgements We thank D. Romero and A. Dondas (Museo Municipal de Ciencias Naturales “Lorenzo Scaglia”, Mar del Plata, Argentina), D. H. Verzi (Museo de La Plata, La Plata, Argentina), and J. Yañez (Museo Nacional de Historia Natural, Santiago, Chile) for allowing access to specimens under their care. We thank D. H. Verzi for discussions on morphological evolution of octodontids, and the members of the Laboratorio de Ecofisiología, Universidad Nacional de Mar del Plata, for their continuous support

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and encouragement. Two anonymous reviewers, and the editor D. Kelt, provided valuable critical comments that improved the manuscript. Financial support was provided by Universidad Nacional de Mar del Plata, CONICET, and Agencia Nacional de Promoción Científica y Tecnológica. Appendix 1. SPECIMENS EXAMINED Octodontid specimens in this study are deposited in the collections of the Museo Municipal de Historia Natural “Lorenzo Scaglia”, Mar del Plata, Argentina (MMMP); Museo de La Plata, La Plata, Argentina (MLP), Museo de Historia Natural, Santiago, Chile (MHNC), and Laboratorio de Ecofisiología, Universidad Nacional de Mar del Plata, Argentina (LEMP). The respective museum-catalog numbers are given. Specimens separated by commas. Ctenomys australis Argentina, Necochea, Parque Lillo LEMP P: 1; 4; 8; 9; 10; 12; 14; 16; 17; 18; 23; 31; 33; 35; 38; 39; 41; 42; 46. CA: 2; 4; 5; 6. MMMP: 3236; 82.240. Ctenomys argentinus Argentina, Chaco, Colonia Benítez MMMP: 2450; 2451; 2452; 2453. Ctenomys azarae Argentina, La Pampa MMMP 2287; 1515; 1595; 1596; 1597. La Pampa, Villarino MMMP: 82-101; 82-164; 82-225. Ctenomys boliviensis LEMP: 129; 137. Ctenomys bonettoi Argentina, Chaco, Colonia Elisa MMMP 0673. Ctenomys dorbignyi Argentina, Corrientes, San Miguel MMMP 3459. Curuzú Laurel MMMP 3432. Berón de Astrada, Mbariguí MMMP 3456; 3452; 3424; 3425; 3426; 3427; 3428; 3455; 3457. Ctenomys haigi Argentina, Chubut, Puerto Madryn MMMP 1925. Ctenomys latro Argentina, Tucumán, Ticucho MMMP 1-87; 2426. Tapia MMMP 2427; 2428; 2500; 2501; 2502; 2807; 2808; 3187; 3188; 3189; 3190. Ctenomys leucodon Bolivia, Depto. La Paz, Comanche LEMP 4999; 5793. Ctenomys magellanicus Argentina, Tierra del Fuego, Colonia Herke MMMP 2500; 2501; 2502; 2808. Ruta 3 km2908 MMMP 2807. Tierra del Fuego MMMP D4M. Ctenomys mendocinus MMMP 2276; 2655; 2711. Ctenomys occultus Argentina, Tucumán, Monteagudo MMMP 3184; 3185; 3186; 3187. Ctenomys opimus Argentina, Jujuy, Tres Cruces MMMP 2202; 3101; 3102; 3103; 3104; 3105. Bolivia, Potosí, Laguna Colorada, Campamento ENDE LEMP 929.


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Ctenomys porteousi Argentina, Buenos Aires, Bonifacio MMMP 1337; 1338 ; 1340; 1343; 1347; 1348; 1350; 1351; 2288; 2289; 2290; 2291; 2292; 2293; 2296; 2297. Ctenomys perrensi Argentina, Corrientes, Yatayti MMMP 2437; 2438. Goya MMMP 2440; 2474; 3136; 3417; 3418; 3419; 3420; 3422; 3423; 3453. Salados MMMP 2447. Ctenomys pundti Argentina, Córdoba MMMP I1658; I1659; I1660; I1661; K1; K33; K38; K43; K48; K51; K52; K62; K68. Ctenomys rionegrensis Argentina, Entre Ríos, Concordia MMMP1961; 1962. Ctenomys roigi Argentina, Corrientes, Costa Manción` MMMP 2410; 2411; 2412; 2442; 2461. Ctenomys talarum Argentina, Necochea, Parque Lillo LEMP CT 4; CT5; CT5D7; CT(14)19; CT(20)13; CT(15)1; CT16(8); CT19; CT7D(9); CT107.88. Ctenomys tuconax Argentina, Tucumán, El Infiernillo MMMP 2429; 2430; 2661; 2960; 2962; 2963; 3182; 3303; 3304; 3305; 3310; 3311; 3342; 3346; 3695. Ctenomys tucumanus Argentina, Tucumán, El Cardillar MMMP 2298; 2300. Ticucho MMMP 3181. Octodon bridgesi Argentina, Neuquen, Parque Nacional Lanin, MLP: 12.VII.88.1; 12.VII.88.2; 12.VII.88.3; 12.VII.88.4; 12.VII.88.5; 12.VII.88.6; 12.VII.88.7. Octodon degus Chile, Santiago, Los Dominicos, MHNC 913; 914; 915; 921; 951; 955; 956; 957. Spalacopus cyanus Chile, El Chisco Norte MMMP 3807. Aconcagua Norte, Papudo MMMP 3583; 3585; 3590; 3591. Santiago, Lagunillas MHNC 702; 704. Aconaemys sagei Argentina, Neuquen, Pampa de Hui Hui MLP 17.II. 92.8; 17.II.92.10. Octodontomys gliroides Jujuy, Tilcara, MMMP 755; 2200; 2532; 3057; 3557; MLP 12VII88.10. Actenomys priscus MMMP 411-M; 497-M; 1567-M; 208-S; 586-S. Ontogenetic sequence of Ctenomys talarum Argentina, Necochea, Parque Lillo, LEMP P: 2; 3; 5; 7; 17; 20; 21; 27; 34; 40; 44; 103; 107; 118; 121; V: 53; 54; 56; 57; 59; I: 74; 77; 79; 80; 93; 94; FA: 2; 4; 5; 7; 8; 9; 11. CT: 1; 4; 5; 17; 19; 21; 5D7; 6D2; 7D9; 17.13.3; 7(55)(4); 14(19); 15(1); 16(8); 20(13); C: 1; 2; 3; J: 1; 2; 4; 5; 6; 7; 136; 147; 141.177; 143.179; 144.180; 145.181; 146.182; 147.183; 152.188; 156.193; 159.195; 162.198; 163.199; 218.

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Ontogenetic sequence of Ctenomys australis Argentina, Necochea, Parque Lillo, LEMP P 1; 4; 8; 9; 10; 12; 14; 16; 18; 19; 22; 23; 24; 28; 29; 32; 33; 35; 36; 37; 38; 39; 41; 42; 43; 45; 46; 48; 50; 51; 55; 62; CA: 18; 19; 20; 20.3.92; 21; 22; 23; 25; 26; 26.6; 28; 81. JUV: 32; 36; 43; 44; 45; 46; 48; 50; 51; 62. Ontogenetic sequence of Actenomys priscus MMMP M: 517; 564; 793; 804; 896; 1231; 1550; 1559; 1560; 1562; 1644; 1645; 2024; 2041; 2073; 2120; 2404. S: 385; 718; 720; 766. LITERATURE CITED Abdala, F., D. A. Flores, and N. P. Giannini 2001 Postweaning ontogeny of the skull of Didelphis albiventris. Journal of Mammalogy 82:190-200. Alberch, P., S. J. Gould, G. F. Oster, and D. B. Wake 1979 Size and shape in ontogeny and phylogeny. Paleobiology 5:296-317. Atchley, W. R., and B. K. Hall 1991 A model for development and evolution of complex morphological structures. Biological Review 66:101-157. Bacigalupe, L. D., J. Iriarte-Díaz, and F. Bozinovic 2002 Functional morphology and geographic variation in the digging apparatus of cururos (Octodontidae: Spalacopus cyanus). Journal of Mammalogy 83:145-152. Begall, S., and M. H. Gallardo 2000 Spalacopus cyanus (Rodentia: Octodontidae): an extremist in tunnel constructing and food storing among subterranean mammals. Journal of Zoology (London) 251:53-60. Biknevicius, A. R., B. Van Valkenburgh, and J. Walker 1996 Incisor size and shape: implications for feeding behaviours in sabertoothed “cats”. Journal of Vertebrate Paleontology 16:510-521. Butler, P. M. 1985 Homologies of molar cusps and crests, and their bearing on assessments of rodent phylogeny. Pp. 381- 401 in Evolutionary Relationships among Rodents: A Multidisciplinary Analysis (Luckett, W. P., and J. L. Hartenberger, eds). Plenum Press, New York, New York, USA. Carlson, B. M. 1988 Patten’s Fundations of Embriology. Interamericana, McGraw-Hill, Mexico, DF. 644 pp.


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