*Department of Biology and Graduate Program in Organismic and Evolutionary Biology;
Department of Biology, University of MassachusettsAmherst;
Department of Wildlife and Fisheries Sciences, Texas A&M University
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Abstract |
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Introduction |
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Although the order Rodentia is diagnosed by several derived morphological traits (Luckett and Hartenberger 1985
), many phylogenetic and molecular evolutionary problems persist. For instance, relationships among major rodent families are confounded by mosaic patterns of derived and primitive morphological traits (Luckett and Hartenberger 1985
). Characteristics of the zygomasseteric structure and jaw musculature have long been used for classifying rodent families and suborders, but many of these structures reveal parallelism and reversals throughout the rodent radiations (Nedbal, Honeycutt, and Schlitter 1996
). Even more surprising is the failure of many recent molecular studies to find strong support for the monophyly of Rodentia (Graur, Hide, and Li 1991
; Graur et al. 1992
; Ma et al. 1993
; Wolf et al. 1993
; Noguchi et al. 1994
; D'Erchia et al. 1996
; Janke, Xu, and Arnason 1997
; Reyes, Pesole, and Saccone 1998
). Perhaps the incongruence between the molecules and morphology is a consequence of the ancient evolutionary history of rodent lineages.
Until recently (Nedbal, Honeycutt, and Schlitter 1996
; Huchon, Catzeflis, and Douzery 1999, 2000
), most molecular studies of rodents consisted of limited taxonomic sampling. It is quite clear that any detailed study of rodent molecular phylogenetics and divergence times requires both increased taxonomic sampling and more molecular data. In this study, new nucleotide sequence data from two nuclear genes, one mitochondrial gene, and previously published molecular data were used to address several questions associated with the rodent radiations: (1) Are divergence times for rodent lineages older than suggested by the fossil record? (2) Do genes differ in their ability to resolve phylogenetic relationships among rodent lineages? (3) Is rodent monophyly supported by an increased amount of nucleotide sequences? (4) What is the sister group to the order Rodentia? (5) How does the molecular phylogeny compare with current morphological interpretations of rodent evolution?
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Materials and Methods |
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Nucleotide Sequencing
All sequences were collected on an ABI 377 automated sequencer (P.E. Biosystems) subsequent to cycle sequencing using Big Dye chemistry and recommendations from the supplier (P.E. Biosystems). The sequences of all primers used for PCR are given in table 1 . PCR conditions for 12S were the same as those described in Nedbal, Honeycutt, and Schlitter (1996)
. The tenth, and final, exon of the growth hormone receptor was examined in all of the taxa, and the 11th exon of the breast cancer susceptibility gene, BRCA1, was examined in a subset of those taxa. For GHR and BRCA1, touchdown PCR was used with the following conditions (Don et al. 1991
): 95°C for 30 s, annealing for 30 s (first cycle at 65°C, with temperature decreased 0.5°C per cycle over 40 cycles), and 72°C for 2 min. GHR and BRCA1 PCR products were purified from 1% low-melting-point agarose gels. All new 12S rRNA, GHR, and BRCA1 sequences (appendix) and alignments (EMBL accession numbers ALIGN_000001ALIGN_000004) were deposited in public databases.
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Molecular phylogenies were derived using PAUP*, version 4.0b2 (Swofford 1999
), and both maximum-parsimony (MP) and maximum-likelihood (ML) analyses. In all cases, a representative of the mammalian infraclass Metatheria was designated as an outgroup. Initially, equal weighting was used for MP analyses. If more than one equally parsimonious topology resulted from equal weighting of sites, individual sites were reweighted in proportion to their rescaled consistency index (Farris 1969
). MP analysis was performed for BRCA1 with the branch-and-bound search option. For GHR and 12S, heuristic searches were performed with at least 20 random taxon additions and tree bisection-reconnection branch swapping. Nonparametric bootstrap analyses (Felsenstein 1985
) were performed with 100 replications, each involving 10 random taxon additions and tree bisection-reconnection branch swapping. ML analyses proceeded in an iterative manner (Sullivan and Swofford 1997
). In all cases, empirically determined nucleotide frequencies and the model of Hasegawa, Kishino, and Yano (1985)
were used. Initial estimates of the transition/transversion ratio and the shape parameter of a discrete gamma distribution (eight rate categories), describing the heterogeneity of rates among sites, were based on an MP phylogeny. For multiple equally parsimonious topologies, parameter estimates were based on the topology with the higher likelihood. After an ML search, parameters were reestimated, and a new search was performed. This procedure was repeated until the topology and parameter estimates stabilized. In every case, the values became stable after the second likelihood search. If feasible, nonparametric bootstrap analyses were performed under a likelihood criterion. Otherwise, rough indications of nodal support were derived from quartet puzzling (Strimmer and von Haeseler 1996
). When determining the statistical significance of the difference in tree length or likelihood between competing phylogenetic hypotheses, the tests of Templeton (1983
; parsimony) and Kishino and Hasegawa (1989
; likelihood) were employed.
Four independent molecular data sets were considered in this study (appendix). Because the question of "combinability" of data sets has not been resolved, two extreme approaches were taken. According to the incongruence length difference test (ILD test; Farris et al. 1995
), GHR, 12S, and vWF are significantly incongruent with each other (P < 0.05). Therefore, each gene was analyzed independently, and individually well supported nodes were considered. However, it still has not been demonstrated that a combination of genes deemed to be "incongruent" results in degradation of phylogenetic accuracy compared with separate analyses (our results indicate the opposite; see below). Therefore, a combined MP analysis of 12S, GHR, and vWF was performed for comparison with the separate analyses. Such a comparison may allow for a maximal exploration of the explanatory power of the available data (Larson 1994
). An ML analysis of the concatenated sequences was not computationally feasible, because when parameters unique to each gene were implemented, the analysis using the Baseml 1.3 program of Yang (1997)
was extremely slow. Tests for heterogeneity in the proportion of nucleotide substitutions among codon sites were performed with the program Monte Carlo RxC 2.21 (B. Engels, personal communication), which determines an empirical P value via the examination of random tables with the same marginal sums generated by a Monte Carlo procedure.
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Results and Discussion |
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Each gene exhibited a unique pattern of evolution. Among the three protein-coding genes, the proportion of substitutions among the three codon positions (table 2
) was significantly different (Monte Carlo procedure, P < 0.001). The highest rate of change and the greatest skew in the rates of substitution among sites ( parameter of the gamma distribution) were observed for 12S rRNA. This is not surprising because the mitochondrial genome has a higher rate of evolution than does the nuclear genome in general, and sites in rRNAs fall into two broad categories: double-stranded stems that change rather slowly, and single-stranded loops that appear to have few constraints on the substitutions that are accepted (with the few exceptions of sites involved in codon or tRNA-synthetase recognition). The next highest rates were displayed by GHR and vWF. Overall, vWF exhibited more bias in its substitution process. The transition/transversion ratio was slightly higher than that for GHR, but both were near the typical ratio of about 2:1 observed for most nuclear genes. However, vWF had greater skew in the distribution of substitution rates among sites (
vWF = 0.55 vs.
GHR = 0.96), with a slightly greater majority (60% vs. 53%) of substitutions occurring at third codon positions. Interestingly, BRCA1 had a rather low rate of substitution and had very little skew in rates of substitution (
= 2.7). However, this may be somewhat biased by the small number of sequences and may change as taxonomic sampling becomes denser. There is almost an equal distribution in the number of substitutions among the three codon positions in BRCA1.
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Both separate and combined analyses provided mixed results regarding rodent monophyly and a sister group relationship between Rodentia and Lagomorpha (superorder Glires). An MP analysis of GHR provided strong support (90% bootstrap) for a clade containing rodents and lagomorphs, yet suggested rodent paraphyly relative to lagomorphs (fig. 1a
). ML results for GHR supported rodent monophyly (54% quartet puzzling), yet only weakly supported (18% quartet puzzling) the monophyly of Glires (fig. 1b
). Although these results are similar to those observed by Huchon, Catzeflis, and Douzery (1999)
, trees that do not support either rodent monophyly or the monophyly of Glires (e.g., MP trees one step longer and ML trees with slightly lower likelihood values) are not significantly worse by the criteria of either Templeton (1983)
or Kishino and Hasegawa (1989)
.
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Previous molecular studies challenging rodent monophyly have included only two to four rodents, and it is possible that the inclusion of additional taxa (e.g., both rodents and nonrodents) would change these results. For example, Reyes, Pesole, and Saccone (1998)
found that rodent polyphyly was the optimal result with available data from complete mitochondrial genomes. Nevertheless, a reanalysis of additional nonrodent mtDNA sequences produced optimal phylogenies with a monophyletic Rodentia in some analyses (personal observation).
The level of support among the analyses for a monophyletic Rodentia may be instructive. 12S rRNA did not support rodent monophyly at all. It is the most rapidly evolving of the four genes and has the greatest skew in rates of substitution among sites. GHR and vWF have intermediate rates of evolution and skew in the distribution of rates and gave moderate support for rodent monophyly (Huchon, Catzeflis, and Douzery 2000
; fig. 1
). BRCA1, on the other hand, has the lowest rate of evolution and very little skew in substitution rates. Some rodent lineages are quite ancient, dating to the early Eocene (Korth 1994
). Given the antiquity of these lineages and a generalized increase in the rate of nucleotide substitution in rodents (Wu and Li 1985
), it is possible that genes exhibiting rates of substitution or biases in the distribution of rates among sites that are near those of GHR and vWF may be accumulating sufficient homoplasy to begin to weaken the phylogenetic signal. In contrast, BRCA1 exhibits a low and fairly homogeneous distribution of rates among sites. This decrease in the amount of homoplasy may explain the unusually strong support BRCA1 gives to rodent monophyly and relationships within rodents. If this is the case, BRCA1 has great promise for rodent systematics and for superordinal relationships among mammals. Future studies of higher-level mammalian systematics should focus on genes with evolutionary dynamics similar to those of BRCA1.
Hystricognaths
Although the separate and combined analyses provided mixed results in terms of diagnosing the monophyly of either Glires or Rodentia, these data did provide strong support for specific rodent associations that have been debated extensively. For instance, the sister group to the suborder Hystricognathi (guinea pig and relatives) has been a long-standing problem in rodent phylogenetics. Although a large number of morphological and molecular traits suggest a sister group relationship between the family Ctenodactylidae and Hystricognathi (George 1985
; Lavocat and Parent 1985
; Luckett 1985
; Sahni 1985
; Wood 1985
; Flynn, Jacobs, and Cheema 1986
; Jaeger 1988
; Beintema et al. 1991
; Martin 1993
; Huchon, Catzeflis, and Douzery 2000
), others disagree (Hartenberger 1985
).
Among the rodents in this study, Ctenodactylus and Pedetes were the only hystricomorphous and sciurognathous taxa. All hystricognaths are ancestrally hystricomorphous. GHR sequences produced very high support values (100% bootstrap and 95% quartet puzzling) for a sister group relationship between Ctenodactylus and hystricognaths, but trees that were contradictory to this sister group relationship were not significantly different under parsimony or likelihood (P > 0.05). Results from 12S were consistent with GHR in an unorthodox manner. According to 12S, Ctenodactylus clustered within Hystricognathi, and this broad clade received weak support. The nesting of Ctenodactylus within hystricognaths is not consistent with morphological data and possibly can be ascribed to homoplasy. In any case, the results for Ctenodactylus were not consistent with Hartenberger's (1985)
suggestion that ctenodactyloids (along with geomyoids) represent the earliest branch among living rodents.
The placement of Pedetes was ambiguous based on single-gene and combined analyses. GHR and the combined analysis grouped Pedetes sister to myomorphs (muroids and dipodoids), and 12S clustered Pedetes with geomyoids, in agreement with previous results from 12S (Matthee and Robinson 1997
). However, bootstrap and quartet puzzling values for those placements were low. BRCA1 placed Pedetes closer to muroids than to Sciurus, Aplodontia, and Graphiurus with strong bootstrap and quartet puzzling support (+19 steps, P < 0.002;
L = 9.3, P = 0.07). This supports Luckett's (1985)
argument that there is not a particularly close relationship between Pedetes and sciuromorphous rodents as has sometimes been suggested (Fischer and Mossman 1969
; Otiang'a-Owiti, Oduor-Okelo, and Gombe 1992
). In general, the weight of evidence from morphology and molecules supports a close relationship of Ctenodactylus with hystricognaths but rejects a close relationship of Pedetes with those taxa.
There are two primary hypotheses for the origin of the hystricognath radiation. Hystricognaths may have originated in North America and dispersed into South America and the Old World (Wood 1985
), or they may have an Old World origin with caviomorphs originating from African phiomorphs (Lavocat 1969
). Both GHR and the combined analysis of GHR, 12S, and vWF support Lavocat's (1969)
hypothesis in that caviomorphs are a monophyletic clade originating within a paraphyletic Phiomorpha. However, phylogenies contradicting the monophyly of caviomorphs are not, or are only marginally, significant under parsimony and likelihood (P
0.05).
In vWF analyses (Huchon, Catzeflis, and Douzery 2000
), Thryonomys/Bathyergus was the basal hystricognath clade, with Trichys sister to caviomorphs. GHR reverses this arrangement in that Hystrix was the basal hystricognath and Thryonomys clustered with Heterocephalus. This arrangement was consistent with the hypothesis that bathyergids originated from thryonomyids (Lavocat 1973
) and with immunological data (Sarich 1985
). However, there was no significant difference (P > 0.05) from trees six steps longer that placed the Thryonomys/Heterocephalus clade basal among hystricognaths. In a combined analysis of GHR, 12S, and vWF, the hystricid lineage was basal, but a tree only four steps longer that placed the Thryonomys/Heterocephalus lineage basal was not significantly different (P > 0.05). To what extent this can be ascribed to the aberrant evolutionary pattern of Thryonomys (Huchon, Catzeflis, and Douzery 1999
) or to homoplasy in the GHR data is unclear. The issue remains unresolved from a molecular perspective.
Dipodoidea and Muroidea
Numerous morphological and molecular studies (Klingener 1964
; Bugge 1985
; Luckett and Hartenberger 1985
; Nedbal, Honeycutt, and Schlitter 1996
; Huchon, Catzeflis, and Douzery 1999
; Michaux and Catzeflis 2000
) support a sister group relationship between muroid and dipodoid rodents. GHR alone and combined GHR, 12S, and vWF sequences provided strong support for this relationship (P < 0.02). For the combined analysis, all trees within 30 steps of the most parsimonious tree that separated muroid and dipodoid rodents either rooted the tree on that branch or rendered rodents paraphyletic with three separate lineages. Both of these scenarios are extremely discordant with other molecular data and with morphology, indicating that the separation of muroids and dipodoids is very unlikely based on combined GHR, 12S, and vWF sequences. For 12S, four trees three steps longer than the most parsimonious tree that placed Pedetes between Jaculus and muroids were not significantly different from the shortest tree (P > 0.05). Therefore, the addition of GHR sequences greatly bolstered previously weak molecular support for Myodonta (Muroidea and Dipodoidea).
Castor and Geomyoids
There are three sciuromorphous lineages of rodents, castorids, sciurids, and geomyoids. GHR analyses placed Castor sister to geomyoids (Geomys, Cratogeomys, and Perognathus) with high bootstrap and puzzling support values but separated Sciurus from these two groups. Nevertheless, trees that separated Castor from the geomyoids were not significantly different (+4 steps, L = 5.2; P > 0.05). Although Sciuromorpha frequently is not regarded as a monophyletic taxon (Dawson and Krishtalka 1984
; Bugge 1985
; Hartenberger 1985
; Luckett 1985
; Wahlert 1985
; Wood 1985
), a sister group relationship between castorids and geomyoids is a novel finding. However, this would be consistent with a North American origin for these two groups (Vianey-Liaud 1985
). A monophyletic Sciuromorpha was only slightly worse and was not significantly different (+2 steps,
L = 8.4, P > 0.05).
Aplodontia, Sciurus, and Graphiurus
A clade containing Aplodontia (protrogomorphous), Sciurus (sciuromorphous), and Graphiurus (myomorphous) appears in analyses of GHR, 12S, BRCA1, and vWF (Huchon, Catzeflis, and Douzery 1999
; but see Huchon, Catzeflis, and Douzery 2000
) and in combined analyses. These three taxa share a number of basicranial traits that support their close relationship (Lavocat and Parent 1985
; Vianey-Liaud 1985
; Wahlert 1985
), and dormice and sciurids are united by B1-dID SINE sequences (Aplodontia was not examined; Kramerov, Vassetzky, and Serdobova 1999
). The support for a glirid/aplodontid/scurid clade was not overwhelming in that the BRCA1 tree separating Graphiurus from Sciurus and Aplodontia was 21 steps longer and significantly different (P = 0.001), but trees that broke up this clade were not significantly different for GHR, 12S, or the combined analysis (P > 0.05). However, the frequent occurrence of this clade in molecular analyses suggests that the association may be real but difficult to support, perhaps due to a short period of common ancestry.
Relative Resolving Power of GHR, 12S, and vWF
Four genes were applied to rodent relationships in this paper. The "combinability" of three of these genes (GHR, 12S, and vWF) was assessed, and they were found to be significantly incongruent (ILD test, P < 0.05). Nevertheless, a concatenation of those three genes produced a phylogeny that was reasonable from a morphological and a paleontological standpoint and was supported with extremely high bootstrap proportions. In the presence of the incongruence, how much confidence can be placed in the total-molecular-evidence tree? Another way of putting this question is to ask if the phylogenetic signal is evenly distributed among the three genes or if one or two of the genes contain relatively little phylogenetic content. If the phylogenetic evidence is more or less evenly split among the genes, then each gene should be viewed as an equally strong hypothesis of relationships, and the separate analyses should be given the greatest credence. On the other hand, if one or two genes are weak, then either the combined result or the relationships constructed from one gene should be given the greatest credence.
Table 4
summarizes a comparison of the optimal parsimony topologies for each gene and for the combined analysis. For the combined data set, the tree of figure 3b
was significantly different from any of the single-gene trees. Similarly, the optimal tree for GHR alone was significantly different from the combined data tree or the best trees for 12S or vWF alone. Interestingly, for 12S and vWF there was not a significant difference between the combined data tree and the tree optimal for either of those genes alone. For vWF, there was also a lack of significance for the difference between the vWF tree and the GHR tree. Which is the "best" phylogenetic hypothesis? We feel that the phylogeny of figure 3b
is the best provisional hypothesis of rodent relationships because it is the one most compatible with the three individual genes (only GHR exhibits a significant difference), and it retains the monophyly of rodents, consistent with morphological data and some other molecular studies (Hasegawa et al. 1992
; Novacek 1992
; Honeycutt and Adkins 1993
; Martignetti and Brosius 1993
; Kuma and Miyata 1994
; Meng et al. 1994
; Frye and Hedges 1995
; Porter, Goodman, and Stanhope 1996
; Cao et al. 1997
; Shoshani and McKenna 1998
; Huchon, Catzeflis, and Douzery 1999
; Liu and Miyamoto 1999
).
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Unequal Rates of Change and Dating Rodent Divergences
Dates of divergence among mammals are highly controversial. Kumar and Hedges (1998)
recently estimated divergence dates for several vertebrate groups. For most mammalian taxa, particularly rodents, these dates are much earlier than those estimated from paleontological data. For example, Kumar and Hedges (1998)
calculated a divergence date of 40.7 MYA and Huchon, Catzeflis, and Douzery (2000)
calculated a date of 41.9 MYA (Equus-Ceratotherium calibration) for Mus and Rattus, whereas fossil data indicate a date no later than 14 MYA (Jacobs and Pilbeam 1980
) and earlier molecular data suggested dates in the range of 530 MYA (Wilson, Carlson, and White 1977
; Sarich 1985
). Kumar and Hedges (1998)
based their dates on a large number of proteins, a molecular clock, and a mammal-versus-bird calibration at 310 MYA. Although Kumar and Hedges (1998)
tested for a molecular clock, the dates concerning rodents are of concern, because rodents are known to demonstrate an acceleration of molecular evolutionary rates (Wu and Li 1985
). Indeed, exactly this pattern was seen for GHR (fig. 4
). The rate of evolution of GHR is very heterogeneous among mammals, with the highest rates of change observed among rodents, and in a likelihood ratio test a molecular clock was rejected (without clock, -ln = 1,2507.5; with clock, -ln = 12,742.1; P < 0.001). Huchon, Catzeflis, and Douzery (2000) based their dates on either linearized trees or quartet dating, often using a fossil-based rodent divergence date for calibration. The inclusion of a rodent calibration point to estimate rodent divergence dates introduces a confounding influence in that a mistake in the calibration will have a uniformly inflating or deflating influence depending on whether the true date was under- or overestimated. We took the approach of calibrating molecular evolutionary rates based on nonrodent divergences that were highly concordant between paleontological and molecular studies followed by explicitly accounting for unequal rates of change among rodents.
A detailed examination of relative rates (Mindell and Honeycutt 1990
) of change (fig. 4
) demonstrates that Monodelphis, artiodactyls, and primates are evolving at clocklike rates but that rodents are evolving at a significantly faster rate. Therefore, it is not feasible to apply a uniform molecular clock to estimate dates of divergence for all mammalian orders. However, one can take advantage of the fact that primates, artiodactyls, and Monodelphis exhibit clocklike rates of change to estimate the absolute rate of change in rodents. Fossil and molecular data concur on two relevant divergence dates: that of apes versus Old World monkeys (i.e., Homo and Macaca;
23 MYA) and that of ruminants versus suids (i.e., Bos and Sus;
65 MYA). Using a Poisson correction of amino acid divergence, the distance between Homo and Macaca is 0.0471 (0.0471/2(23) = 0.001/Myr), and the distance between Bos and Sus is 0.172 (0.172/2(65) = 0.0013/Myr). The average of these two rates is 0.00115/Myr.
By assigning branch lengths to four-taxon trees (fig. 4b
; Monodelphis, primates, and two ingroup taxa), one can establish the relative rate of change of GHR among rodent lineages and assign dates to their divergences (table 3
). These dates show concordance with fossil-based dates and a recent analysis of 87 separate genes (W.-H. Li, personal communication), whereas the dates of Kumar and Hedges (1998)
do not. This is surprising, because our method for assigning dates implements a similar strategy to the one employed by Kumar and Hedges (1998)
, in that both use a "lineage-specific method." Both methods underestimate the real rate of evolution in rodents, because the period of rodent common ancestry preceding the rate acceleration is included in the estimation of evolutionary rate. However, our use of a mammal reference (primates) should underestimate the rate acceleration less drastically than Kumar and Hedges' (1998)
use of a bird outgroup because of the shorter period of common ancestry following the primate-rodent divergence than that following the bird-rodent divergence.
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Functional Changes in GHR
The action of the growth hormonegrowth hormone receptor complex has been studied in a diversity of mammals, including Mus, Rattus, and Cavia (the guinea pig). Remarkably, the guinea pig is completely unresponsive to both its own and exogenous growth hormone, and its growth is totally unaffected by the absence of growth hormone (Mitchell, Guillemin, and Selye 1954
). Despite this finding, it is clear that the guinea pig secretes a functional growth hormone, because it has somatotropic action in hypophysectomized Rattus (Knobil and Greep 1959
). The extracellular domain of GHR binds growth hormone of other species, indicating that the lack of growth hormone responsiveness does not involve a reduction in binding affinity (Amit et al. 1992
; Ymer, Stevenson, and Herington 1997
). On this basis, it has been suggested that the lack of effect of growth hormone in Cavia is due to a defect in postreceptor signaling (Harvey and Fraser 1992
; Keightley and Fuller 1996
). We sequenced exon 10, which encodes the entire intracellular domain of the growth hormone receptor in a large number of mammals. As was found previously (Adkins, Vandeberg, and Li 2000), the intracellular domain of GHR of Cavia and of other hystricognath rodents is not unusually divergent in amino acid sequence (fig. 4
). Growth hormone and the extracellular domain of GHR of Cavia are also highly conservative (Adkins, Vandeberg, and Li 2000). Therefore, it seems likely that the lack of responsiveness to growth hormone displayed by Cavia is due to a defect in intermediate messengers, such as STAT5, JAK2, or the growth-promoting insulin-like growth factor I, whose secretion is stimulated by growth hormone. Study of these proteins in Cavia might elucidate the abnormal response of the guinea pig to growth hormone. In this context, it is fascinating to note that Cavia has 10 times the normal level of insulin in its circulation and that its insulin molecule possesses growth-promoting activity (King and Kahn 1981
). Is it possible that insulin has replaced the normal physiological function of growth hormone in the guinea pig, perhaps through interaction with the receptor for insulin-like growth factor I.
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Acknowledgements |
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Footnotes |
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1 Keywords: Rodentia
molecular phylogeny
divergence dates
2 Address for correspondence and reprints: Ronald Adkins, Department of Biology, 221 Morrill, University of Massachusetts, Amherst, Massachusetts 01002. radkins{at}bio.umass.edu
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