Evolution, 40(1),1986, pp. 94-106
COMPARATIVE PATTERNS OF GROWTH AND DEVELOPMENT IN CRICETINE RODENTS AND THE EVOLUTION OF ONTOGENY
G. KEN CREIGHTON' AND RICHARD E. STRAUSS Museum ofZoology and Division ofBiological Sciences, University ofMichigan, Ann Arbor MI 48109
Abstract. - The quantitative description ofgrowth curves for morphometric traits provides a basis for assessing the ontogenetic patterns underlying differences in morphological struc ture, as demonstrated with comparisons among neotomine-peromyscine rodents. Morpho metric differences among contemporary rodent species are shown to result from relatively simple changes in relative growth rates and timing. Quantitative ontogenetic studies add a dynamic component to the assessment ofmorphological similarity, thus providing a more robust procedure for detecting homoplasy than static comparison of adult morphology. Applying the principles of phylogenetic systematics to studies of developmental timing among closely related taxa may be a useful and informative complement to studies based on molecular similarity or static comparison of adult morphology. Interspecific and intra specific differences in allometric scaling ofanatomical structures may reflect differences in growth patterns among the taxa compared; caution is warranted in inferring patterns of genetic correlation from data on phenotypic scaling.
Received March 12, 1984. Accepted July 16, 1985
Contemporary and traditional classi larity in adult morphology reflects simi fications of higher vertebrates are based larity in the underlying patterns and pro in large part on assessments ofsimilarity cesses ofdevelopment (Bonner and Hom, in adult structure of living and fossil 1982). This presumption of develop forms. Two assumptions underlie all in mental conservatism is more amenable ferences about patterns of relationships to study (at the gross morphological level) based on comparative evidence, whether with contemporary techniques. We can the basis ofcomparison is phenetic (based describe and evaluate differences in size on overall similarity) or phylogenetic and shape of morphological features in (based on derived similarity or synapo terms of relative rates and timing of morphy) and whether the data are mor growth in an appropriate number ofmor phological or molecular. The first as phological dimensions. What is required sumption is that degree of phenotypic is a method ofdescribing growth in terms similarity is related to degree of genetic ofindividual ontogenies that can be used similarity. Though perhaps sustainable to affect comparisons among a broad for some primary gene products and enough range oftaxa to be interesting and macromolecules (such as hemoglobins informative. and cytochromes), this is largely untested We present here a quantitative analysis for most complex structures in verte of patterns of growth and development brates and may be difficult to test in prin in a suite offive morphometric traits and ciple (Dawid et al., 1982; Lewontin, four "discrete" developmental land 1984). An observed lack ofcorrelation in marks for 13 species (eight genera) of some cases has caused problems for sys North American cricetine rodents. That tematists andevolutionarybiologists (e.g., differences in size and shape of homol Turner, 1974; Schnell et al., 1978; Les ogous structures in different taxa result sios, 1981). from differences in rates and timing of The second assumption is that simi- growth and development is axiomatic (Alberch, 1980). In providing quantita 'Current address: The Nature Conservancy, In tive descriptions of age-specific growth ternational Program, 1785 Massachusetts Avenue, patterns, however, we will show how N.W., Washington, DC 20036. similarity in size and shape ofadult mor- 94 COMPARATIVE ONTOGENY OF RODENTS 95 phological features may arise from dif and Master, 1983), but the mean values ferent patterns of development and as approximate the general pattern ofgrowth sess the degree to which differences in in these features for a typical individual "control parameters" (sensu Alberch et ofa given taxon. Indeed, studies of"tar al., 1979; Alberch, 1980) underlie the ob geted" growth (Tanner, 1963) in rodents served diversity in adult morphology. (Riska et al., 1984; Atchley, 1984) and Subsequently, we will summarize differ ofheritabilities ofgrowth parameters (Ei ences in the relative timing of develop sen, 1975; Herbert et al., 1979; Kidwell ment of various traits among these ro et al., 1979) indicate that growth rates dents, outline a program for using such may be tightly regulated about this av data to estimate phylogenetic relation erage, converging on a very restricted ships among them, and compare the phy range of adult phenotypes within a pop logeny estimated from comparative on u1ation. Estimates ofadult size were based togenetic data with alternatives estimated either on measurements of wild-caught from more traditional studies based on specimens (generally the parents of the static comparison of adult morphology. sample) or on the asymptotic size cal Finally, we show how differences in the culated from the growth curves for a par relative rates and timingofgrowth in var ticular sample (Fig. 1). Unlike some mu ious traits (e.g., brain and body weights) rid rodents, neotomine-peromyscines may account for the patterns ofstatic al exhibit no detectable sexual dimorphism lometry observed in some intraspecific in any of the traits studied (Carleton, and interspecific comparisons. 1980), so samples included both male and female young. Data were also recorded on the mean MATERIALS AND METHODS length ofthe gestation period and on the The Quantitative Description ofGrowth timing ofthree "discrete" developmental Data. -Our study is based on longi events: eye opening, ear opening, and tudinal data reported in the literature for eruption of the lower incisors. We rec 13 species ofneotomine-peromyscine ro ognize that the characterization of these dents, representing eight ofthe 18 genera latter events as discrete is arbitrary in recognized by Carleton (1980) (Table 1). that they represent recognizable points We included all species of neotornine along a developmental continuum; we use peromyscine rodents for which complete the term merely to imply a repeatably data sets were available. In addition, we and unambiguously observable land included, for comparison, data on two mark in the development of an animal. other species of rodents: Perognathus These events also correspond with sig longimembris (Heteromyidae) and Rat nificant phases in the life history of ro tus exulans (Murinae). dents, such as attainment ofthe abilities Complete data sets included informa to orient to their environment acousti tion on postnatal growth in five metric cally or visually and to process solid food. features: bodyweight (W), head and body Analytical Methods. -Comparison of length (HBL), tail length (TL), hind foot data on growth and development among length (HFL), and ear length (EL). Data taxa requires a model for describing were reported in the literature as means growth that is sufficiently precise to char for a study sample, measured at weekly acterize individual trajectories, yet suf intervals or less, for at least the period ficiently flexible to facilitate inter-taxon from birth to eight weeks ofage (e.g., Fig. comparisons. The parametersrequired to 1). Obviously many factors, such as litter describe and compare patterns of post size, age and condition of the mother, natal growth in a given trait, such as body differential mortality of smaller young, weight, are shown in Figure 2. Our for and laboratory conditions, influence the malism and terminology are generally growth rates ofindividual young (Myers consistent with Alberch et al. (1979). 96 G. K. CREIGHTON AND R. E. STRAUSS
TABLE 1. Taxa, sample sizes, adult body weight, and literature references for data on growth and development in rodents.
Taxon NO Weight (g) References Cricetinae Neotoma albigula 4-11 149.2b Richardson, 1943 Ochrotomys nuttalli 8 18.3c Layne, 1960 Ototylomys phyllotis 86 65.5b Helm, 1975 Peromyscus leucopus castaneus 111-158 21.9b Lackey, 1973 Peromyscus leucopus noveboracensis 80-185 19.6b Lackey, 1973 Peromyscus maniculatus bairdUd 39 15.5b Svihla,1935 Peromyscus maniculatus artemisiae 14-63 21.3c SvihIa, 1934 Peromyscus melanocarpus 21-41 59.0b Rickart, 1977 Peromyscus mexicanus 7-17 60.5b Rickart, 1977 Peromyscus yucatanicusl 45-108 28.6b Lackey, 1976 Podomys floridanus- 20 27.3c Layne, 1966 Reithrodontomys humulis 7-20 6.0b Layne, 1959 Scotinomys tequina 93-140 14.8b Hooper and Carleton, 1976 Scotinomys xerampelinus 44-80 14.7b Hooper and Carleton, 1976 Tylomys nudicaudus 9.5 284.3 b Helm, 1973 Heteromyidae Perognathus longimembris 26 8.2b Hayden and Gambino, 1966 Murinae Rattus exulans 7-28 73.0c Wirth, 1973 a Minimum and maximum sample sizes for each age interval from birth to 8 weeks. b Weight of lab-raised specimens at last age recorded. C From wild-caught specimens. dAdditional data from Dice and Bradley (1942) and Layne (1968).
However, our descriptions of ontogeny partitioned, in terms ofthree parameters: are grounded in a quantitative, general size at birth (SOl); growth rate (K); and the ized model of negative exponential length of the growth interval (fJ - a). growth (von Bertalanffy, 1960; Laird, Choosing 90% of asymptotic size to 1965) (Fig. 2A). In this model a repre represent fJ, or a comparable point such sents the time ofonset ofgrowth (or birth, as 95% or 99%, provides a landmark from in our study); SOl is size at birth; fJ is de within the range of observed data that fined as the age (time since birth) at which indicates the age at which a constant pro 90% ofexponential growth (Laird, 1965) portion of total exponential growth has has occurred; SfJ is that corresponding occurred. When the data are well fit by a size; and SAis the asymptotic (adult) size negative exponential model there exists at the end of the period during which a unique function that describes the tra growth approximates a negative expo jectory through the points (a, SOl)' (fJ, SfJ) nential curve. k. is the average growth with an asymptote at SA, so that we can rate over the interval from birth (a) to represent the curvilinear growth trajec 90% adult size (fJ). A consistent notation tory with a straight line segment ofslope is used to describe growth trajectories of k.(the average growth rate, Fig. 2A) with the other traits; for example, HBLfJ is 90% no loss of information. of adult HBL while fJHBL is the age at Negative exponential growth curves which that size is attained (Fig. 2B). When were fit to the data using a robust non the model holds for a given morpho linear regression procedure that involves metric trait, these few parameters pro fitting the model exactly to all possible vide a complete and precise description subsets ofthree data points and selecting of postnatal growth. The difference in the medians of the parameter distribu adult size between any two forms in a tions thus generated. This is a modified particular trait can be accounted for, or jackknifing (subsetting) technique which COMPARATIVE ONTOGENY OF RODENTS 97
tI,SA ------ sp ------100
R ..... °50 .L: C, C Q) --l
II Time p (Birth)
B. 70 10 15 Reithrodontomys Age (weeks) HBLA ------;;------FIG. 1. Growth offour linearly measured traits E HBlp ------..s from birth through 15 weeks ofage for Peromyscus .s: i, (Podomys) jloridanus. Bars indicate range of mea '& 40 l j I surements at each age. N = 20. Redrawn from Layne I I (1966). I I Mean square error: 1.31 :I Residual autocorrelation =0.03 I ,I , i) yields approximate maximum-likeli '0 , I hood estimates ofthe explicit parameters I of the von Bertalanffy model (to, SA, k); 20 p_ 30 40 50 60 ii) provides comparable estimates ofad Time (days) ditional, biologically important descrip FIG. 2. A) Descriptive parameters for general tive parameters (such as ex, (3, Sa,and Sfj); ized negative exponential (Bertalanffy) growth curve and iii) provides robust estimates of the (see text for discussion). B) Fitted postnatal growth curve, corresponding equation, and statistics offit sampling errors of these parameters and for head and body length (HBL) of Reithrodonto ofthe covariances among them. Thus we mys humulis. can describe each ontogenetic trajectory by a few biologically interpretable de scriptive characteristics for which we also birth to eight weeks of age. This vector have estimates of variances and covari provides a convenient and consistent ances. measure of overall size and provides a In the same way that we describe standard measure against which growth growth curves for individual traits, we in individual traits can be compared. A can evaluate and compare the ontoge measure of the equivalence of the size netic trajectories of multivariate vectors vectors among taxa is provided by the computed from some combination of coefficients of vector correlation (Chev logically or functionally related features. erud, 1982) for pairwise comparisons of We represent "general size" in our com taxa. This statistic is the cosine of the parisons by a vector summarizing the angle between each vector pair, calculat joint size increase in all morphometric ed as the inner product of the loadings traits (Jolicoeur, 1963; Leamy and Brad (Morrison, 1976). For normalized vec ley, 1982). Our general-size vector is the tors (or those roughly equal in scale), this majoraxis (first principal component, PC value equals unity when the vectors are I) calculated from the covariance matrix parallel and zero when they are orthog oflog-transformed mean values for each onal. Among the 15 taxa vector corre age sample, representing the interval from lations ranged from 0.972 to 0.999, in- 98 G. K. CREIGHTON AND R. E. STRAUSS
E 50 A. ..s IZO A. as B Olotylo~ II ~ E. Pmeloflocorpu$ 100 5 20 ~ 80 .s: j 15 Podomys ~ 60" Vi ..8 15 10 • >. 40 -0 40 L1' • C .. g 109 , ::g :// :z: o,---,--:':"""----:':----:"..-~ ~ 15 20 25 ...J ...... lD . r ~90 C. D. J: P.mellicanus ./" i!l /' ~80 Podomys CQ. 30 ~ r=O.80 g.70 ~60 ~50 ~ 40 Reilhrodonlomys • o i:r ~::: 10 15 20 25 "-,-0"'---"'-""''''-'''''''''' 7,0 7,5 8.0 8.5 9.0 Time (days) Time (days)
FIG. 4. Pairwise comparisons of postnatalgrowth ...J lD B. in several measurements. A) Difference in size at J: 98 ~ CQ. •• • birth and postnatal growth rate in head and body -e___---z..• •• _ length (HBL) for Ototylomys phyllotis and Reithro -C •• dontomys humulis. B)Difference in postnatal growth elf 96 • rates for foot length between Peromyscus melano • carpus and Podomys jloridanus. C) Difference in '0 • duration ofgrowth in general size (within-group PC ~ 94 I) between Peromyscus mexicanus and Ototylomys C nuttalli. D) Difference in size at birth, average growth C r=-O.l4 rate, and duration of growth in HBL for P. jlori -Q) danus and R. humulis. ~ 92 Q) o 0.. 6.0 6.5 7.0 7,5 8.0 8.5 9.0 length (HBL), for example, is not related Adult Size (SA) to overall size among these taxa, as in FIG. 3. The relationship between the A) abso dicated by the lack of any significant re lute and B) relative timing of growth in head and lationship between absolute adult size and body length (HBL) for 16 rodent taxa from Table the proportion ofadult size (S,J at which 2. A) The age (3HBL as a function of general adult size (SA based on within-group PC I). B) The per HBL,s is attained. centage ofadult size (S~ attained at time (3HBL, as Differences among taxa in the relative a function of adult size. Data from Table 2. Open adult size of a given feature may result circles represent Ototylomys phyllotis. from three general types of ontogenetic differences: differences in size at birth (Fig. 4A); differences in average growth rates dicating relatively high consistency for (Fig. 4B); differences in the duration of this measure of overall size. the geometric growth phase (Fig. 4C); or some combination ofthese (Fig. 4D). The RESULTS AND DISCUSSION terminology ofAlberch et al. (1979) can Differences in Growth Patterns be used to describe these differences in Among Species growth pattern. Figure 4A illustrates a The absolute duration of growth in situation ("displacement") in which adult most traits surveyed for these rodents is differences are influenced primarily by the strongly correlated with body size (e.g., timing of onset of exponential growth. Fig. 3A); larger rodents, in general, take Figure 4B illustrates the consequences in longer than smallerrodents to reach adult terms ofadult morphology ofdifferences size. However, the relative timing ofpar in relative growth rates only, to which ticular traits (expressed in terms of pro the terms "acceleration" or "neoteny" portion of general adult size) is mostly would apply depending on the phyloge independent ofbody size (Fig. 3B). Rel netic context (Fink, 1982). In Figure 4C, ative timing ofgrowth in head and body changes in the timing ofoffset (duration) COMPARATIVE ONTOGENY OF RODENTS 99
100 A. ~~~ , 6.5 P.m. artemisiae 90 Reithrodontomys 80 6.0 70 Ui" Perognathus - Ochrotomys - 5.5 Q) 60 N ---Reithrodontomys (jj 6.0 B. 50 ~ 5.0 c: Q) (!) A 8 C 0 E F G H 4.5 ev N 100 'Vi ..... 90 :J -0 o 80 . 15 20 ...... r/'" 0 70 10 20 30 40 50 60 ev -Neotome Time (days) g 60 ---Tylomys FIG. 5. A) Growth curves for multivariate size 'E ev 50 estimates (S) for Peromyscus m. artemisiae, Rei ....o throdontomys humulis, and Perognathus longi ev 0.... A B C 0 E F G H membris. B) Average growth rates (k) from birth (a) to (3 for the same taxa. 100 , .... ~- ,...."" 90 ...... ofgrowth result in morphological differ 80 ences attributable to "progenesis" or 70 "hypermorphosis," again depending on - P. yucatanicus the phylogenetic context. The difference 60 --- Ototylomys in HBL between adult Podomys flori 50 danus and Reithrodontomys humulis (Fig. 4D) is due to composite differences in the ABCDEFGH prenatal ontogeny, postnatal growth rate, Developmental Events and duration ofgrowth. It is perhaps best FiG. 6. Pairwise comparisons of relative timing characterized by direct comparison ofthe of developmental events during ontogeny. Events growth trajectories. We can partition the (A-H) are from Table 2. Lower-incisor eruption was not used due to incomplete data. difference in HBL between these taxa into three components: difference in prenatal ontogeny (.:lex), postnatal growth rate (tJ<.), postnatal growth rate, and duration of and duration ofgrowth (.:lfJ). Comparing growth. Such differences might reflect rel growth patterns in this way is useful for atively recent selection on life history understanding the way selection may have traits (such as length ofgestation) or may operated on various aspects ofgrowth to represent differences due to phylogenetic effect differences in adult morphology. history. The comparison of growth in overall We have seen that, while the absolute size (within-group PC I score) among the duration of growth in these traits is three taxa illustrated in Figure 5 shows strongly correlated with body size, rela both convergence (R. humulis vs. Perog tive timing (expressed in terms of pro nathus Iongimembrist and divergence portion of adult size) varies indepen (Peromyscus m. artemisiae vs. R. hu dently of body size. To compare overall mulis) in body size during postnatal de developmental patterns, we plotted the velopment. Again, differences in adult percentage of general adult size (S) at size among these taxa can be partitioned which each of eight developmental into differences due to prenatal ontogeny, "events" or landmarks occurred for sev- 100 G. K. CREIGHTON AND R. E. STRAUSS
TABLE 2. Relative timing of nine developmental landmarks expressed in terms of percentage of adult size (SA)' Standard deviations (SD) and coefficients of variation (CV) are based on arcsine-transformed proportions.
Developmental landmarks Auditory f3 f3 f3 meatus Eyes foot ear f3 tail f3 Lower- Birth open open length length HBL length WI incisor Taxon (A) (B) (C) (D) (E) (F) (G) (H) eruption Neotoma albigula 62.5 82.0 88.8 92.5 94.0 96.6 99.3 99.9 Ochrotomys nuttalli 60.5 78.0 83.8 90.6 98.8 98.1 96.9 99.3 70.0 Ototylomys phyllotis 76.7 no 81.3 93.6 96.6 91.4 90.2 97.0 o.o- Peromyscus I. castaneus 56.8 79.0 81.2 93.4 95.9 98.2 98.1 99.6 65.0 Peromyscusl. noveboracens~ 56.8 80.0 83.4 94.8 95.8 97.5 97.6 99.3 67.0 Peromyscus maniculatus 53.5 78.3 84.3 94.6 94.8 95.8 98.7 99.6 68.0 Peromyscus melanocarpus 54.7 85.0 89.1 92.9 95.9 95.7 99.2 99.5 77.0 Peromyscus mexicanus 56.9 83.0 86.1 93.1 96.1 94.8 98.7 99.9 76.0 Peromyscus yucatanicus 55.2 82.0 85.3 92.1 95.9 97.6 98.2 99.5 72.0 Podomys floridanus 52.6 80.0 85.8 94.6 94.8 97.0 98.6 99.2 Reithrodontomys humulis 59.9 82.0 82.1 94.2 98.9 96.5 97.4 99.7 no Scotinomys tequina 57.8 84.0 86.1 93.6 96.8 97.0 98.0 99.7 Scotinomys xerampelinus 59.2 84.0 84.2 92.9 96.5 97.1 97.9 99.2 Tylomys nudicaudus 74.5 81.0 83.5 96.1 96.1 97.1 97.8 99.4 o.o- Perognathus longimembris 50.6 81.0 81.4 92.0 95.0 96.3 95.4 98.2 Rattus exulans 59.0 77.0 80.4 94.3 94.5 97.5 97.7 99.5 71.0 SD 4.3 1.8 2.1 1.6 2.3 2.3 3.2 2.0 2.8 CV(%) 8.5 2.9 3.1 2.1 2.9 2.8 3.9 2.4 4.9 Number of taxa 16 16 16 16 16 16 16 16 9 a Erupted at birth(Helm, 1973).
eral pairwise comparisons (Table 2, Fig. allimitations (e.g., pelvic breadth) on size 6). This type of plot provides a conve of young at birth, and other ecological nient visual summary ofsimilarities and and physiological compromises. contrasts between the patterns ofrelative developmental timing among taxa, in Inferring Phylogeny from Quantitative dependent of body size. The ordering of Ontogenetic Data events (A through H ofTable 2) was as Developmental patterns, like other as signed to be the ontogenetic sequence ob pects of the phenotype of contemporary served in Rattus exulans, a murid rodent organisms, have an historical compo outside ofthe primary study group. This nent; that is, they may reflect (in part) the ordering is consistent with the most com evolutionary history ofthe animals stud mon ontogenetic sequence within the ied. The data of Table 2 comprise a ma neotomine-peromyscines. trix of information on similarities and The relative amount ofvariation in rel differences in developmental patterns ative timing of the eight developmental analogous to a matrix ofcharacters used events and landmarks is summarized in in conventional taxonomic studies. To Table 2. Size at birth exhibits the largest evaluate the pattern of phylogenetic re amount ofvariation, likely reflecting dif lationships implied by these data on rel ferences in absolute and relative gesta ative timing, we computed a Wagner net tion lengths. The factors affecting the work (Kluge and Farris, 1969; Farris, tradeoff between the proportion of total 1970) (Fig. 7A) and rooted it based on developmental time spent in utero vs. ad the conclusions of Carleton (1980) (Fig. mamma are likely to be complex, in 7B). This network ofsimilarity in devel volving relative risks of predation to opmental timing can be viewed as an hy pregnant females and nestlings, structur- pothesis of phylogenetic relationship COMPARATIVE ONTOGENY OF RODENTS 101 among the neotomine-peromyscines. The A. numbers plotted on the tree identify par simonious locations of switches or re versals in the relative order ofoccurrence oftwo developmental events. i I When taken at face value, these data on heterochrony show a moderate degree of homoplasy comparable to most tradi tional morphological data sets. Consider B. ing only the relative order of occurrence of discrete developmental landmarks gives a consistency index (Farris, 1970) of 0.5. This low level of fit, however, is primarily an artifact ofcharacterizing re versals in an arbitrary, typological man ner: reversals were identified as switches Apomorphies in the relative order ofoccurrence oftwo I. HBL'-"ail 2.HBL_eClf 3.80r_l0il landmarks without regard to the type of 4.Ioil _toot change in developmental pattern (accel 5HBL
A.Corleton 11980) B.Hooper and Musser11964) PeromysCU$ 5J.
70 +O/aly/amys xNeotoma • P. yuco1onicus • P. mexicanus a> N • P.melanocarpus U'i ~ « 30 ~ 0 to 20 30 o 40 a> 0' FIG. 9. Hypothesized phylogenies for 14 neo o C 90 tomine-peromyscines from A) Carleton (1980) and ~ B.Ear length B) Hooper and Musser (1964), reduced to include a> 0... only the taxa studied here. Relationships among 70 Peromyscus spp. are inferred from Hooper's (1968) classification. Square bracket encloses species of Peromyscus sensu lato, after Hooper (1968). 50
30 velopmental patterns of Ototylomys and Tylomys with other neotropical crice 10 tines (e.g., the sigmodontines). o 10 20 30 ~ Despite the wide range of body sizes Age (days) and ecological habits represented by the FIG. 8. Average growth rates (K) from birth (a) seven species and subspecies of Pero to f3 for A) head and body length and B) ear length, for six neotomine-peromyscine taxa. See text for myscus (sensu lato) included in this study, discussion. ouranalysis based on relative timing sup ports the notion that the genus (along with Podomys) is monophyletic. Inclusion of on conventional morphological compar Podomys in Peromyscus is contrary to ison (Fig. 9), but differs in some details. the conclusions ofCarleton (1980) but in As in Carleton's (1980) study, Ototylo agreement with most previous (Hooper, mys and Tylomys are highly divergent 1960, 1968) and subsequent (Rogers, from the otherneotomine-peromyscines. 1983) studies. In fact, they are more different from the It is not our intent to imply that these other taxa than is the Pacific murid, Rat few taxa and characters studied provide tus exulans. Hooper (1960), Hooper and a rigorous basis for revising the classifi Musser (1964), and Carleton (1980) have cation of neotomine-peromyscines. remarked on the distinctiveness ofthese Rather, we compare ourresults with those genera, and Carleton (1980) suggested derived from more traditional methods that they either represent an early off to illustrate the information content of shoot ofthe neotomine-peromyscine ra data on developmental timing and to em diation or are independently derived from phasize its potential utility in phyloge North American eumyine stock. Their netic studies. These nine "characters" highly divergent pattern of timing in provide a relatively well resolved picture growth and development is consistent ofinterrelationships that is consistent in with Carleton's conclusion that their major outline with previous studies. common ancestry with the other neo An assumption underlying most clas tomine-peromyscines is remote. In this sification systems, and virtually all at context it would be interesting and po tempts at phylogeny reconstruction based tentially informative to compare the de- on comparative evidence, is that devel- COMPARATIVE ONTOGENY OF RODENTS 103
opmental programs are conservative and 20 relatively stable-i.e., that morphologi cal similarity reflects similarity in the ge netic component of the developmental 10 1000 program. The correspondence between CD E 8 JY-- 800 0 C' the estimates of general relationships _ 6 , s // ...... --...--..... ------600 ~ from this study, based on relative timing, s: / y"" C' and more conventional studies, based on -iii .0-'" / .... ~ ~------static comparison of adult morphology, 3: 4 Brain wI. 400 :r >. u 3 is consistent with this general assump o lCl lD 3 tion. One advantage ofevaluating the on - P.m. bairdi; 2 200 togeny ofmorphological traits is that in --- P.m. gracilis stances in which similarity in adult structure results from different underly ing developmental trends (convergence) Il,.--+-_o---+---+_-+---+-_-+--_--.:IIOO can be identified (Fig. 5). Furthermore, o 10 20 30 40 by evaluating the patterns ofmorpholog Age (days) ical change during ontogeny, we may dis FIG. 10. Postnatal growth in brain weight and cern the way selection has altered growth body weight for Peromyscus m. bairdiiand P. graci patterns to affect the variation that we lis showing difference in (3's for brain weight. Data observe in adult morphology (Guerrant, from King and Eleftheriou (1960). 1982). genetic correlation between brain size and Growth Curves and Allometric Scaling body size; and ii) the similarity ofscaling The ubiquity ofregular size-scaling in within and between populations might interspecific and intraspecific compari simply reflect the consequence of selec sons ofmorphological structure has long tion or random drift acting on body size, been recognized (e.g., Snell, 1891) and with brain size secondarily affected to the abundantly documented (Huxley, 1932; degree that it is genetically correlated with Gould, 1966, 1975; McMahon, 1973). body size (see also Leamy and Atchley, Laird (1965) elucidated the basis for the 1984). While Lande's inferences are con frequently observed log-linear allometry sistent with commonly observed patterns of growth in terms of the mathematical of intraspecific scaling in these features, relationship between the underlying the proximate mechanism underlying growth curves of the structures com these regular patterns remains unex pared. One of the most well known and plained. thoroughly documented allometric rela Differences in intraspecific scaling of tionships in vertebrates is the log-linear brain size with body size may result from scaling ofbrain size with body size (Jer heterochronic shifts in growth patterns ison, 1973). For comparisons among (Gould, 1977). For example, the data of mammalian taxa spanning even a mod Figure 10 represent mean growth curves est range of body sizes (e.g., primates or ofbrain weight and body weight for lab rodents), the scaling coefficient for brain oratory-raised samples oftwo ofthe sub size with body size in intergeneric com species of Peromyscus maniculatus dis parisons approximates 0.67, while in in cussed above. The growth trajectories for traspecific comparisons (within or be body weight are indistinguishable, as is tween populations) the coefficient is the trajectory for brain weight from birth typically in the range of 0.2 to 0.4 (Jer until about eight days of age. After that ison, 1973). Lande (1979), in evaluating age the growth trajectories for brain data on small rodents, suggested that i) weight diverge. The allometric relation the lower coefficient typically observed ships between brain weight and body in intraspecific studies might reflect the weight from day 10 through day 40 are 104 G. K. CREIGHTON AND R. E. STRAUSS
40 cease growing (forward shift in fJ) at dif 2. 30 20 0 0 0 0 ferent ages. Scaling identical to that shown P m. graci/is in Figure 11 would result from compar ison of adult animals whose growth was I. E 0 truncated at various points along the 0'500 mean trajectories of brain and body S 40• x:+ weight, simultaneously. Finally, pheno 0' 30 2s 'w 20• typic correlations may reflect underlying ;: genetic correlations to the extent that c '0 • P. m. bairdii these are manifest by changes in the over " 10 all rate or timing of growth that affect cD 400 o both characters simultaneously (e.g., pleiotropy). •10
350~~ --:-__~ ~.....J ACKNOWLEDGMENTS 4.5 5 6 7 8 9 10 15 Body weight (qrn) We have appreciated, enjoyed, and FIG. II. Log-log plot of postnatal allometry in benefited from discussions with M. D. brain weight vs. body weight for Peromyscus m. Carleton, W. L. Fink, M. A. Houck, D. bairdii (closed circles) and P. m. gracilis (open cir J. Klingener, A. G. Kluge, P. Myers, J. cles) from 10 to 40 days ofage (labeled points). L. Patton, G. R. Smith, R. S. Voss, and members ofthe Museum ofZoology Sys plotted in Figure II. Allometric coeffi tematics Discusion Group and the Mor cients for P. m. bairdii and P. m. gracilis phometrics Study Group, concerning are 0.21 and 0.37, respectively, spanning various aspects of the methods, results, the typical range for intraspecific allo and interpretions presented here. Mi metric scaling in these features (Lande, chael Carleton generously provided us 1979; Gould, 1971). The observed dif with his original data on Scotinomys. Fi ferences in ontogenetic allometry ofbrain nancial support from the Division ofBi and body weight are a consequence of a ological Sciences and the Museum ofZo difference in the timing ofoffset in cranial ology, University ofMichigan, and from growth. Atchley et al. (1984) have pro NSFgrants DEB-8011562 (R.E.S. and G. posed a physiological model to account R. Smith) and BSR-8307719 (R.E.S. and for such changes in cellular proliferation. F. L. Bookstein) is gratefully acknowl Several inferences can be drawn from edged. this comparison. First, caution must be LITERATURE CITED exercised in deriving conclusions about ALBERCH, P. 1980. Ontogenies and morphological genetic correlations from data on phe diversification. Amer. Zoo!. 20:653-667. notypic scaling (see Atchley and Rut ALBERCH, P., S. J. GOULD, G. F. OSTER, AND D. B. ledge, 1980; Cheverud et aI., 1983). The WAKE. 1979. Size and shape in ontogeny and phylogeny. Paleobio!. 5:296-317. patterns of phenotypic correlations ob ATCHLEY, W. R. 1984. Ontogeny, timing of de served in mixed longitudinal series of velopment, and genetic variance-covariance specimens may simply reflect the age dis structure. Amer. Natur. 123:519-540. tribution of the sample (Cock, 1966). In ATCHLEY, W. R., B. RISKA, L. A. P. KaHN, A. A. natural populations with asynchronous PLUMMER,ANDJ. J. RUTLEDGE. 1984. Aquan titative genetic analysis of brain and body size breeding, fluctuating resource availabil associations, their origin and ontogeny: Data ity, and differential size-related mortali from mice. Evolution 38:1165-1179. ty, such heterogeneity is to be expected ATCHLEY, W. R., AND J. J. RUTLEDGE. 1980. Ge (Myers and Carleton, 1981). In animals netic components ofsize and shape. I. Dynamics ofcomponents ofphenotypic variability and co with relatively determinant growth (e.g., variabilityduringontogeny in the laboratory rat. most mammals) allometric trends may Evolution 34:1161-1173. also reflect comparison among adults that BERTALANFFY, L. VON. 1960. Principles and the- COMPARATIVE ONTOGENY OF RODENTS 105
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