Akberch 1983 Morphological Variation in the Neotropical Salamander Genus Bolitoglossa

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Morphological Variation in the Neotropical Salamander Genus Bolitoglossa Author(s): Pere Alberch Source: Evolution, Vol. 37, No. 5 (Sep., 1983), pp. 906-919Published by: Society for the Study of EvolutionStable URL: http://www.jstor.org/stable/2408406Accessed: 13-03-2015 18:55 UTC

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Evolution, 37(5), 1983, pp. 906-919

MORPHOLOGICAL VARIATION IN THE NEOTROPICAL SALAMANDER GENUS BOLITOGLOSSA

PERE ALBERCH Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts 02138

Received September 15, 1982. Revised November 30, 1982

There are two aspects to any process of evolutionary change. One is the probability of survival of any given trait within a given context (i.e., other traits present in the individual and in the population, physical environment, population structure, etc. . . .). That is, the probability of fixation of a trait under the action of natural selection and stochastic processes. The other aspect is the nature, and origin, of the variation upon which the agents pre- viously mentioned can operate. Mutation and recombination have been the mechanisms traditionally invoked in the generation of variation at the genetic level. However, selection operates at the level of the phenotype and, therefore, it is justified to ask if the properties of the variation at the genetic level can be extrapolated to the phenotypic level, particularly to the level of complex morphologies.

Recently, Ho and Saunders (1979), Al- berch (1980, 1982a, 1982b), Gould (1980), Rachootin and Thomson (198 1), Oster and Alberch (1982) and Wagner (1982) among others have contended that there are qual- itative differences between modes of evolution at the genetic and epigenetic levels. A simple gene-phenotype extrapolation would only be correct if there were a one- to-one correspondence between a given morphological trait and a given region of DNA in the genome. This is obviously not the case. Morphology is the product of complex, and very often regulatory, genetic and epigenetic interactions. By epigenetic I mean interactions among gene products and their environment, not, as often assumed, nongenetic. These developmental interactions constrain the expression of morphological variation upon which natural selection operates. At the morphological level, one can abstract these

processes and view phyletic phenotypic change as the result of genetically mediat- ed regulation of a resilient developmental program.

The present study addresses the above issue from an empirical perspective. I ask the question: What kind of phenotypic variation do we find in natural populations? However, I purposely do not focus on quantitative variations in metric traits as is often done (e.g., Lande, 1976; Chev- erud, 1982). Rather, I analyze the variation encountered in osteological characters used in taxonomy and systematics. Tax- onomists have chosen these traits, not because of their adaptive properties, but due to the diagnostic properties of these discrete and highly invariant traits. Further- more, when paleontologists discuss evolution above the species level in the fossil record, they are basically studying the patterns of change in these species-diagnostic traits. Since the paleontological def- inition of species is based on purely morphological criteria, analyses of mechanisms of morphological change of such features among extant species can be readily ap- plied to actual macroevolutionary patterns in the fossil record and related to contem- porary controversies (e.g., Stanley, 1979).

I describe the intra-specific (mostly intra-populational) variation found in the dermal bones of the nasal region, and in the number of tarsal elements and phalanges in various species of the neotropical salamander genus Bolitoglossa. This is a highly diverse genus, characterized by its adaptive radiation into the New World tropics (see Wake and Lynch, 1976, for an introduction to the genus).

The main conclusion of this paper is that the variation encountered is characterized by a recurrence of the same variants in

906


MORPHOLOGICAL VARIATION IN BOLITOGLOSSA 907

n p nld

1 mm ~ max

FIG. 1. Dorso-lateral view of the anterior cranial elements of a cleared and double stained adult Bol- itoglossa rostrata, illustrating the generalized condition in the genus. The cartilaginous nasal capsule is lightly stained as compared with the darkly stained dermal bones. The eye socket (eye has been removed in this preparation) is located in the lower right hand side of the figure. pm-ascending processes of the premaxillary; f-frontal; max-maxilla; p-prefrontal; n-nasal, nld-naso-lacrimal duct foramen.

widely unrelated species. This pattern, when coupled with ontogenetic information, agrees with the view of morphological diversification occurring by regulation of a resilient developmental program.

MATERIALS AND METHODS Post-embryonic ontogenetic series of the

following species were prepared: Bolito- glossa adspersa, B. altamazonica, B. dofleini, B. occidentalis, B. peruviana, B. platydactyla, B. rostrata and B. subpalmata. The specimens had their soft tissues cleared with KOH after trypsin treatment and their skeletal tissues stained with Alizarin Red for calcium deposits in bone and Alcian Blue for cartilage (the method slightly modified after Dingerkus and Uhl- er, 1977, and Wassersug, 1976). A list of the specimens observed and their size is given in Appendix 1.

All the morphological observations and scoring of the character states were done by the author using a stereomicroscope. All characters discussed were photo- graphed for documentation and in some cases (particularly in the study on the an-

n nasal eye V:~~~~~ ~~ copsule

max. Irnm

B. plofydoctylo FIG. 2. Lateral view of the anterior cranial re-

gion in Bolitoglossa platydactyla (FMNH 70165). Note the reduced ossification as compared with Fig- ure 1. The prefrontal does not articulate with any neighboring element. Cartilage-stippled; foramina-dark stippling. See Figure 1 for abbreviations. en-external naris.

terior cranial elements) camera lucida drawings were made to assist in the analysis of the data. There are many unsolved taxonomic problems in some groups of Bolitoglossa, particularly the identity of somewhat differentiated allopatric populations. For example, Wake et al. (1982) discuss this problem in B. altamazonica and B. peruviana. For this reason I have tried whenever possible to obtain the study series of any given species from a single population. Phylogenetic problems relat- ing to Bolitoglossa and allied genera are discussed in Wake and Lynch (1976) and Wake and Elias (1983). Elias (1983) and Larson (1983a, 1983b) specifically discuss intra-generic relationships in the Bolito- glossa beta group, while Hanken and Wake (1982) discuss the systematics of some species of the alpha group.

RESULTS Anterior Cranial Region

Morphology of the Anterior Cranial Ele- ments in Primitive Bolitoglossa.-The prefrontals are paired dermal bones that occur on each side of the skull of urodeles immediately anterior to the orbit. They are


908 PERE ALBERCH

~1/

Imm

B. G/IcmGzonrcc FIG. 3. The most paedomorphic condition is en-

countered in small species like this Bolitoglossa altamazonica (KU 128585), where the prefrontal is absent. Cartilage-stippled.

the last dermal bones to appear during the ontogeny of the Bolitoglossa skull (Al- berch and Alberch, 1981) and they are the only skull bone whose presence is inter- specifically variable within Bolitoglossa. No lacrimals or septomaxillae are typical- ly found in the genus, although Wake (1966 p. 15) reports the abnormal presence of septomaxillae in two specimens of B. rufescens, one B. mexicana and one B. platydactyla. The prefrontals are elongated in shape and are relatively small. They usually lie on top of the cartilaginous nasal capsule. The condition in adults of primitive species is shown in Figure 1. The other bones in the nasal region of Bolito- glossa are the paired nasals, the paired maxillae and the single premaxilla. The nasal bones are of particular interest to this study because of their developmental interactions with the prefrontals. The nasals are relatively large dermal bones that curve over the antero-lateral surface of the nasal capsule.

The naso-lacrimal duct, forming much earlier during ontogeny than the sur- rounding dermal bones, is an important landmark to interpret the various bone ar- rangements. A fairly constant arrange-

Imm

S. peruvlano FIG. 4. Dorso-lateral view of the anterior cranial

region in Bolitoglossa peruviana (KU 124127).

ment is to have the naso-lacrimal duct bounded anteriorly and dorsally by the nasal, posteriorly by the prefrontal and ventrally by a sulcus between the anterior and posterior ascending processes of the maxillae (Fig. 1). Noble (1921) provides additional discussion on the morphology of the anterior cranial elements in plethodontid salamanders.

Derived conditions in Bolitoglossa are characterized by a progressive reduction of ossification. In particular, the prefrontals become reduced and "float" on top of the cartilaginous nasal capsule, i.e., they do not articulate with any neighboring element (Fig. 2). In the most derived state, the prefrontals have been lost (Fig. 3).

Ontogeny of the Anterior Cranial Ele- ments, with Emphasis on the Prefron- tals.-The homologies and geometric patterns of the anterior cranial bones are difficult to interpret due to the highly epigenetic nature of their development (e.g., Devillers and Corsin, 1968). There is a large degree of independence between cytodifferentiation and growth of individual elements. For example, if a bone fails to differentiate (or is experimentally removed, as in Corsin, 1968), the neighbor-



TABLE 1. Intrapopulational variation (adults).

Prefrontal

Both sides Species N present One side Absent

B. rostrata 12 12 0 0 B. subpalmata 14 11 0 3 (F) B. adspersa 12 2 2 8 (F) B. platydactyla 8 6 1 1 (F and ABS) B. dofleini 14 7 5 2 (F and ABS) B. altamazonica 5 0 0 5 (ABS) B. peruviana 7 0 3 4 (F?) B. occidentalis 12 0 1 11 (ABS)

ing bones can invade the "territory" of the missing bone. For example, Figure 4 il- lustrates a case where the prefrontal bone (apparently absent in this specimen of B. peruviana) has had its presumptive area partially invaded by the neighboring nasal and maxillary process. The normal condition in B. peruviana is very similar to the one found in B. altamazonica (Fig. 3). Therefore, it is impossible to conclusively interpret the morphology of the anterior cranial elements by simply observing the adult stage. In the specific case illustrated in Figure 4, one cannot definitively conclude that the prefrontal is really absent or that, instead, has fused with one of its neighboring bones. The only way to re- solve the issue is by studying ontogenetic series. In Appendix 2, I describe in some detail the ontogeny of B. adspersa, which represents the most complex pathway found in the genus.

Variation.-The observed patterns of variation in the adult specimens of the various species studied are summarized in Table 1. "Absent" means that a prefrontal is not observed; that can include either true absence of the prefrontal or fusion. I tried to distinguish between these two conditions by studying ontogenetic series (Fig. 5). If the lack of the prefrontal is due to fusion, one should expect to encounter a stage during ontogeny where the prefrontal is present. This is the case in B. adspersa (see Appendix 2), B. subpalmata and B. platydactyla. Conversely, the condition in B. occidentalis and B. altamazonica is due to the fact that the prefrontal fails to

differentiate (Fig. 5). Bolitoglossa dofleini and B. peruviana are more difficult to interpret. Based on an inspection of the ontogenetic pattern in B. dofleini, it appears that in most of the adults the observed single element is the result of a fusion. However, in some instances the territory of the prefrontal is unossified, giving the impression that the condition results from the absence of prefrontal ossification. We might be dealing with a mixed process where in some individuals the prefrontals form and subsequently fuse with the nasals, while in some other cases they fail to differentiate. In B. peruviana, only juveniles (with one exception) show prefrontals present in one side, while most adults lack prefrontals. The tentative conclusion is that they have resulted from fusion, although we cannot exclude that they have failed to differentiate and the nasals and maxillae have invaded the prefrontal territory (Fig. 4). Wake et al. (1982) also point out the presence of tiny prefrontals in some specimens of B. peruviana. The possibil- ity that differential survival of the various morphs during ontogeny may play a role in the generation of the B. peruviana pattern cannot be excluded given the small sample size considered. I consider this hypothesis unlikely. In the other species, although one lacks longitudinal data, the pattern is clear in the sense that the youngest specimens in each series are not polymorphic for the trait; rather, they all lack the bone that has yet to differentiate. Larger, but still immature, specimens exhibit prefrontals, although sometimes


910 PERE ALBERCH

PRES - 0 0 oo o0o 00 000o 0 0 PRES - ooooo 000 0 0 00

1/2 - 0 0 1/2 - 0000

ABS o o 00 ABS - 0 0 00 I I I I I I I I I I I I

10 20 30 40 50 60 70 10 20 30 40 50 60 70

8 odsperso S 0/0tydoctyl/o PRES - 0 0 0 PRES - 000 00

1/2 ! 0 0 1/2 - 0 0

ABS - o 0 0 00 00 ABS - o 0 0 I I I I I I I I I I I I

10 20 30 40 50 60 70 20 30 40 50 60 70 80

PRES PRES - 0 00 0 0 0 0

1/2 - 0000 0 1/2 - 0 0 0 00

ABS - 00 0 0 ABS - o o I l ~ ~I l I , I I , I 10 20 30 40 50 60 70 10 30 50 70 90 110 130

mm mm FIG. 5. Absence (ABS), presence on just one side (1/2) or presence on both sides of the skull (PRES) of

the prefrontal bones in relation to body length (S.V.L.) in various species of Bolitoglossa.

asymmetrically. The presence/absence variation is found in the adults.

Other Variation in Anterior Cranial Elements. -The described polymorphism of the prefrontal bone is the only variation observed in this study involving the presence or absence of a dermal bone. In ad- dition, in one specimen of B. adspersa and one of B. occidentalis, I observed the par- tial fusion of the ascending processes of the premaxilla. This is a condition not characteristic of any species of Bolitoglos- sa; however, it is diagnostic of a variety of plethodontid genera (Wake, 1966).

Autopodial Region Tarsal Morphology.-The distal tarsals

are the most variable bones found in the Bolitoglossa tarsus. The only additional variation, beyond the number of distal tarsals, found in this survey was one B. rostrata with a fusion of the intermedium and fibulare. The primitive condition

found in Bolitoglossa is three distal tarsals (Fig. 6b). Tarsals 1 and 2 are assumed to be fused in all urodeles (Fig. 6a), while the fusion of tarsals 4 and 5 is a diagnostic trait for the genus Bolitoglossa (Wake, 1966). Therefore, the primitive condition is Tarsale (1 + 2)131(4 + 5), as illustrated in Figure 6b. This is the morphology most commonly found in B. rostrata, B. subpalmata, B. adspersa, B. platydactyla, B. altamazonica and B. peruviana. In fact, this is the condition found throughout the genus, except in the rufescens group and in B. dofleini. Also, it has been reported in the poorly known B. veracrucis (Wake and Brame, 1969) and observed in the highly variable B. mexicana and B. hart- wegi. The derived condition found in those species results from the fusion of distal tarsal 3 with the already fused tarsal 4 + 5, i.e., these species exhibit only two distal tarsal elements ((1 +2)/(3 + 4 + 5)), as shown in Figure 6c. The intraspecific



Primitive Condition in Plethodontidae Primitive Condition in Bo/i6oq/ossa Derived Condition in Bo/itog/ossa

7~~~~j7 PF>(7 1~~~~~~~~~~~mm 6 b-

I Tmm i t Imm i

FIG. 6. Trends in the variation of distal tarsals (stippled elements) in Bolitoglossa.

variation found in distal tarsal arrange- ment is summarized in Table 2. The per- centages are probably not significant due to the relatively small sample sizes. The important point is the recurrence of the same morphologies while some others are never encountered. The distribution is certainly nonrandom, as was already discussed in Alberch (1980). The values given here quantitatively, but not qualitatively, differ from the ones given in Alberch (1980). This discrepancy is due to larger sample sizes and to the restriction to single populations in this study.

Phalangeal Morphology. -In the species analyzed the phalangeal morphology was highly constant. The generalized phalangeal formula is 1,2,3,3,2. Some paedomorphic species have lost the terminal (third) phalange of the fourth digit. For example, Alberch and Alberch (1981) discussed the case of the progenetic species B. occidentalis. I refer to the number of phalanges regardless of their histological condition (i.e., cartilage or bone). In some specimens, particularly in B. platydactyla, B. dofleini, B. peruviana, B. occidentalis and B. altamazonica, the terminal elements are extremely reduced and re- main cartilaginous. This cartilaginous condition of the terminal elements has caused many discrepancies in the literature where phalangeal formulas were given based on X-ray or alizarin stained specimens. In those cases only ossified phalanges were reported. I found in this study the number of phalanges to be a

highly invariant character. The only variation encountered was found in three specimens of B. altamazonica out of nine examined that had three phalanges in the fourth digit. The condition was asymmet- rical, i.e., found on only one foot.

CONCLUSIONS

An analysis of the patterns of variation presented above readily suggests some regularities that can be discussed sepa- rately.

Patterns Restricted Variation. -Not all possible

phenotypes were found. In fact, only a very limited subset was observed. The prefrontal was the only element in the anterior region of the skull exhibiting variation in terms of presence or absence; the compo- sition of the other elements was invariant. The reason is not obvious. A priori, and from a strictly genetic perspective, a mutation could affect any bone. This is not the case. In species, like B. occidentalis, that 'have lost the prefrontal, the only variation found is the occasional presence of that bone (Table 1). I never did find a septomaxillary or a lacrimal (skull bones that are absent in Bolitoglossa) or any new bone. Furthermore, one never finds losses of any other element but the prefrontal. Similarly, in the case of tarsal morphology, there are 16 possible tarsal arrange- ments, based on fusions and divisions of the distal tarsals. Of these possibilities, only three are observed. It is very difficult


912 PERE ALBERCH

TABLE 2. Intrapopulational variation in tarsal morphology.

Tarsal Condition (% distribution)

4 tarsals 3 tarsals 2 tarsals Species N (5,4,3, 1 +2) (5 +4) (5 +4 +3)

B. rostrata 48 3 97 0 B. subpalmata 42 7 93 0 B. adspersa 29 0 93 7 B. platydactyla 24 0 87.5 12.5 (Interpopu-

lational variation)

B. dofleini 34 0 17 83 B. occidentalis 44 0 0 100 B. altamazonica 16 0 100 0 B. peruviana 18 0 78 22

to interpret these patterns from an adaptive perspective. Although the morphs observed are probably not maladaptive, one could come up with many other variations that would be equally functional. An adaptive explanation would be even more difficult to give in cases where the "abnormal" morphology is present only on one side of the animal but not on the other (e.g., Figs. 5 and 7). A similar example of bounded phenotypic variation involving the relationship between foot types and tendon types in birds is discussed by Rai- kow (1983). Hence, I conclude that variation is constrained and that the origin of these constraints should be searched for among historical explanations and consid- erations about the internal organization of the organism.

The presence of a prefrontal bone in Bolitoglossa occidentalis might represent an interesting case of atavism. The evolutionary polarity, based on outgroup comparisons, of the morphological trans- formation is from presence of prefrontal (Fig. 1) to absence of prefrontal (Figs. 3 and 7). Bolitoglossa occidentalis is among the most derived species of Bolitoglossa (Wake and Brame, 1969; Larson, 1983). It is characterized by the absence of prefrontals. This represents a true loss of the element since ontogenetic series show that it never differentiates during ontogeny. Alberch and Alberch (1981) have shown that loss of the prefrontal is due to the heterochronic truncation of development

(progenesis). However, in one adult specimen on one side (Fig. 7) a tiny prefrontal has been found. It is very unlikely that the prefrontal has been maintained as a very low percentage polymorphism in this species, since this is the only case observed in approximately 30 adult specimens from various populations. I propose a developmental explanation for this phenomenon in section II. Hansen and Tanner (1958) and Wake and Brame (1969) also report one case of a B. occidentalis with prefrontals present.

Parallelisms between Intraspecific and Interspecific Variation.-Another striking fact that emerges from the data is that all cases of intrapopulational variation in- volve morphs found as characteristic features of other species. For example, the separation of tarsals 4 and 5 found as an anomaly in some B. rostrata (D. Wake, pers. comm., has recently found another case of unfused tarsals 4 and 5 in B. ma- crinii) is the ancestral condition of most generalized urodeles. This observed parallelism between population level anom- alies and species-specific variation suggests that the mechanisms involved in the generation of the observed anomalous variation are the same ones involved in the generation of raw variation for evolutionary morphological diversification.

Mechanisms The underlying hypothesis throughout

the morphological analysis presented here



wxn U max a m , FIG. 7. Cleared and stained adult Bolitoglossa occidentalis exhibiting the normal morphology in terms

of absence of the prefrontal (pf bone in the left hand side of head (b), while an atavistic tiny prefrontal is present on the opposite side (a). See Figure 1 for abbreviations.

is that the observed patterns of variation are not necessarily a reflection of some di- rect environmental selection but that, rather, they are the result of the structural organization of the intrinsic mechanisms generating the trait. In other words, the definitively bounded variation is the result of constraints imposed by the way the organism develops.

With regard to the polymorphisms in tarsal morphology, one cannot say very much, since not enough is known in terms of its ontogeny. The number of tarsal elements may be the result of a series of fusions, as was proposed by Holmgren (1933) and, based on regeneration studies, by Al- berch (1980, unpubl.), or it can be the product of differential spatial determina- tion of cartilage foci, as proposed by Hinchliffe (1977). In the latter case, fusions would not be involved and we would be essentially dealing with a problem of pattern formation. Due to the lack of ad- equate numbers of early embryos of Bol- itoglossa, I cannot discuss the mechanistic basis of the observed tarsal variation.

There is very good evidence for sug- gesting heterochrony as the mechanism controlling the patterns of variation re- garding presence or absence of prefrontals and the terminal (third) phalanges of the fourth toe. As was shown by Alberch and Alberch (198 1) in the highly paedomorphic species B. occidentalis, the prefrontals and the third phalanx of the fourth toe are

among the last ossification events in the ontogeny of Bolitoglossa. Therefore, they are expected to be the features to be lost in paedomorphic species. In fact, they are (Table 1 and Results). However, there is a point where species with intermediate degrees of paedomorphosis should be polymorphic for the trait. This is what we observe. The generalized, and conse- quently less paedomorphic, species always have prefrontals present (although in some cases they may be fused) and a full phalangeal complement. Similarly, the most paedomorphic species studied,* B. occidentalis, is also the least variable. There was no variation in digital or tarsal morphology and only one specimen, out of about 30 examined, had a tiny prefrontal on one side of the skull (Fig. 7).

This relationship between patterns of variation of skeletal elements and degree of paedomorphosis is diagrammatically illustrated in Figure 8. It can be argued that morphological evolution of these traits is the indirect result of differential degrees of paedomorphosis among the various species. Paedomorphosis, and hetero-

* Degree of paedomorphosis in Bolitoglossa was qualitatively established using the traits studied in Alberch and Alberch (1981) and Alberch (1981). These traits are a combination of overall reduced ossification, loss of terminal phalanges, small size and in- terdigital webbing.


914 PERE ALBERCH

o 0

.4: -o

( n

Do r 0

Non-poedomorphic sp. Intermediate polymorphic sp. Poedomorphic sp.

totvisms

DEGREE OF PAEDOMORPHOSIS

FIG. 8. Diagram representing the proposed relationships between degree of paedomorphosis and expected populational variation. The cytodifferentiation of the prefrontal is a discrete phenomenon and it is repre- sented as a threshold. A population is composed of individuals normally distributed with respect to their degree of development (or, inversely, their degree of paedomorphosis).

chrony in general, is clearly related to important life history and fitness parameters such as body size and timing of first re- production (Gould, 1977). It is very plausible to envision that natural selection acts on these "gross" morphological features and that many structural components "tag" along in the process. These changes can be accommodated due to the regulative properties of developmental systems (Al- berch, 1982b) or to selective neutrality. The most important point is that evolution by regulation of developmental programs (as in paedomorphosis) has the following properties: First, paedomorphosis is a non- specific phenomenon, in the sense that it can result due to genetic mutations affect- ing various physiological parameters (e.g., rate of mitotic divisions, hormone production, cell membrane receptors, etc. ...). Therefore, it is likely to occur several times independently. Systematic studies, using biochemical techniques, carried out by Larson (1983) on the Bolitoglossa-beta subgeneric assemblage appear to support

the independent occurrence of similar heterochronic changes in unrelated lineages. Second, every time paedomorphosis occurs, the same set of derived features should be expected, i.e., resulting in extensive convergence and parallelism. Again, this feature characterizes Bolito- glossa evolution (see Wake and Lynch, 1976; Larson, 1983). Analyses in terms of heterochrony pose an interesting paradox. On one hand, they provide an analytical framework within which one can formu- late testable hypotheses. Given the ontogeny of any species, one can predict the expected degree and kind of intraspecific variation to be encountered. For example, elements appearing later in ontogeny should be more variable than traits de- veloping earlier. On the other, a heterochronic analysis is highly phenomenolog- ical, since it does not address the specific genetic and developmental mechanisms that control timing and rates of development. In fact, this paradox is largely a reflection of the communication gap be-



tween evolutionary and developmental bi- ologists, since heterochrony, despite its proven relevance to evolutionary biology, has not received much attention from ex- perimental embryologists.

SUMMARY

Recent models have suggested that the evolutionary dynamics of processes of morphological change are qualitatively different from processes of genetic change, the main difference being that the expression of the phenotype is the product of complex genetic and epigenetic interactions during development. The structure of these interactions results in a non-random apportionment of the morphological variation upon which natural selection can operate. Furthermore, an understanding of the mechanisms controlling ontogeny allows for predictions of what patterns of variation should be expected. To address these ideas, a survey on the patterns of morphological variation found in populations of various species of the neotropical salamander genus Bolitoglossa was un- dertaken. In particular, a series of traits involving the presence or absence of bones in the anterior region of the skull, in the tarsus, and in the toes was analyzed. These represent osteological characters traditionally used by taxonomists working with this group. It has been found that: 1) variation is definitively bounded and 2) traits observed as variants in a population of a given species are found fixed in other species (i.e., population polymorphisms parallel interspecific diversity). It is argued that the patterns observed can largely be explained mainly as the products of heterochronic regulation of resilient developmental programs. Furthermore, it is plausible to view this as the kind of variation that provides the raw material in processes of evolutionary morphological diversification. But, most importantly, the variation observed is clearly non-random and it is largely a reflection of the structure of the developmental program which im- poses constraints on its expression. There- fore, an understanding of ontogeny can al-

low us to make some predictions about phylogeny.

ACKNOWLEDGMENTS

I would like to especially thank David B. Wake for critically reading this manuscript and for placing at my disposition his extensive collections of Bolitoglossa, de- posited in the Museum of Vertebrate Zo- ology, University of California, Berkeley. I also want to express my gratitude to W. E. Duellman (Museum of Natural Histo- ry, University of Kansas), and Harold Voris, Hymen Marx and A. Resetar (Field Museum of Natural History, Chicago) for allowing me to prepare ontogenetic series from material under their care. Michael Bell, Douglas Futuyma and James Han- ken provided suggestions and criticisms that greatly improved the paper. I ac- knowledge with thanks the illustrations by Laszlo Meszoly, photography by A. Cole- man (Museum of Comparative Zoology) and the preparation of the manuscript by Catherine McGeary. Emily Gale and Glenn Flores provided technical assis- tance. This work was partly supported by NSF Grant DEB-81-20917.

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. 1981. Convergence and parallelism in foot morphology in the neotropical salamander genus Bolitoglossa. I. Function. Evolution 35:84-100.

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. 1982b. The generative and regulatory roles of development in evolution, p. 19-36. In D. Mossakowski and G. Roth (eds.), Environmental Adaptation and Evolution: A Theoretical and Empirical Approach. G. Fischer-Verlag, Stutt- gart.

ALBERCH, P., AND J. ALBERCH. 1981. Hetero- chronic mechanisms of morphological diversification and evolutionary change in the neotropical salamander, Bolitoglossa occidentalis (Am- phibia: Plethodontidae). J. Morph. 167:249-264.

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916 PERE ALBERCH

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Corresponding Editor: D. J. Futuyma



APPENDIX 1 List of specimens studied as ontogenetic series (it does not include comparative material from other populations or other species).

Bolitoglossa adspersa. Cundinamarca, Colombia MVZ 62965 (15.5 mm), MVZ 143662 (19.7 mm), MVZ 143643 (27.8 mm), MVZ143634 (24.8 mm), MVZ 83703 (33.5 mm), MVZ 143661 (24.4 mm), MVZ 163581 (35.5 mm), MVZ 143641 (41.6 mm), MVZ 143647 (41.6 mm), MVZ 143650 (44.8 mm), MVZ 143649 (47.3 mm), MVZ 143646 (50.0 mm), MVZ 143655 (46.6 mm), MVZ 143645 (51.7 mm), MVZ 143654 (59.2 mm).

Bolitoglossa altamazonica. Para, Brasil KU 129916 (19.9 mm), KU 129914 (24.3 mm), KU 127289 (27.9 mm), KU 129910 (25.6 mm), KU 129905 (29.9 mm), KU 128598 (32.9 mm), KU 128585 (40.1 mm), KU 128595 (36.7 mm), KU 127296 (40.0 mm).

Bolitoglossa dofleini. Alta Verapaz, Guatemala MVZ 161786 (15.7 mm), MVZ 161788 (16.5 mm), MVZ 161779 (18.7 mm), MVZ 161781 (19.8 mm), MVZ 161618 (37.8 mm), MVZ 161774 (42.6 mm), MVZ 161751 (44.0 mm), MVZ 161766 (47.6 mm), MVZ 161736 (57.3 mm), MVZ 161722 (66.6 mm), MVZ 161731 (65.0 mm), MVZ 161617 (55.1 mm), MVZ 161616 (58.4 mm), MVZ 161606 (76.4 mm), MVZ 161603 (86.0 mm), MVZ 161607 (88.4 mm), MVZ 161605 (92.9 mm), MVZ 161602 (99.5 mm).

Bolitoglossa subpalmata. Cerro de la Muerte, Costa Rica MVZ 114090 (18.5 mm), MVZ 114061 (19.4 mm), MVZ 114094 (20.6 mm), MVZ 114001 (21.7 mm), MVZ 114095 (22.7 mm), MVZ 114088 (25.4 mm), MVZ 114093 (25.5 mm), MVZ 114078 (28.0 mm), MVZ 113978 (29.6 mm), MVZ 113974 (30.4 mm), MVZ 114108 (36.9 mm), MVZ 114105 (38.3 mm), MVZ 113979 (38.9 mm), MVZ 114013 (43.3 mm), MVZ 114117 (51.5 mm), MVZ 113880 (47.6 mm), MVZ 113997 (56.3 mm), MVZ 113900 (56.4 mm), MVZ 114002 (55.4 mm), MVZ 113937 (57.2 mm).

Bolitoglossa occidentalis. Chiapas, Mexico MVZ 130144 (19.4 mm), MVZ 114864 (20.8 mm), MVZ 165306 (23.0 mm), MVZ 100876 (23.5 mm), MVZ 108825 (27.5 mm), MVZ 113141 (29.2 mm), MVZ 100834 (31.3 mm), MVZ 108824 (32.1 mm), MVZ 108820 (34.7 mm), MVZ 100826 (33.1 mm), MVZ 108810 (34.3 mm), MVZ 108805 (37.1 mm), MVZ 161124 (35.1 mm), MVZ 165301 (37.0 mm), MVZ 100852 (39.1 mm), MVZ 100874 (39.8 mm), MVZ130143 (19.3 mm).

Bolitoglossa peruviana. Napo Prov., Ecuador KU 124039 (19.2 mm), KU 152254 (22.1 mm), KU 124126 (22.2 mm), KU 124127 (23.9 mm), KU 124060 (24.5 mm), KU 152252 (32.0 mm), KU 124086 (28.4 mm), KU 124090 (27.3 mm), KU 124068 (41.2 mm), KU 124082 (34.6 mm).

Bolitoglossa platydactyla. Veracruz, Mexico FMNH 124251 (26.5 mm), FMNH 70144 (35.3 mm), FMNH 70083 (34.2 mm), FMNH 70124 (39.5 mm), FMNH 70101 (39.1 mm), FMNH 70146 (42.0 mm), FMNH 70157 (44.4 mm), FMNH 70165 (65.9 mm), FMNH 70111 (44.9 mm), FMNH 70077 (42.9 mm), FMNH 70067 (78.0 mm), FMNH 70113 (42.5 mm). MCZ 8377 (56.5 mm), MCZ 24704 (74.5 mm).

B olitoglossa rostrata. San Marcos, Guatemala MVZ 132227 (13.2 mm), MVZ 132210 (22.9 mm), MVZ 132217 (23.8 mm), MVZ 132224 (22.6 mm), MVZ 132219 (23.8 mm), MVZ 132213 (26.8 mm), MVZ 132214 (27.4 mm), MVZ 132171 (34.0 mm), MVZ 132190 (34.0 mm), MVZ 132205 (34.7 mm), MVZ 132162 (38.7 mm), MVZ 132149 (41.1 mm), MVZ 132140 (47.3 mm), MVZ 132154 (48.2 mm), MVZ 132127 (57.2 mm). MVZ 132143 (56.4 mm), MVZ 132132 (67.2 mm), MVZ 132146 (55.4 mm), MVZ 132134 (59.6 mm), plus four untagged hatchlings (10.0 mm-10.4 mm).

* Size of specimens indicated within parentheses refers to snout to vent length. MVZ = Museum of Vertebrate Zoology, University of California, Berkeley; KU = Kansas University Natural History Museum, Lawrence; FMNH = Field Museum of Natural History, Chicago, MCZ = Museum of Comparative Zoology, Harvard University, Cambridge


918 PERE ALBERCH

APPENDIX 2

Description of Bolitoglossa adspersa nasal/prefrontal ontogeny

The nasal is the penultimate dermal bone to differentiate in the sequence of appearance of dermal elements. At the earliest stage studied (S.V.L. [snout to vent length] = 15.5 mm), the nasals are already forming as thin leaf-like membranous ossifications over the middorsal region of the nasal capsules (Fig. Al). In this specimen, the nasals appear to form from three distinct centers of ossification on one side and two on the other. The presence of separate foci of ossification has only been observed in this specimen (in the young specimens of other species the differ- entiating nasal always appears to have a single ossification center). It is not clear if the specimen illustrated in Figure Al can be considered representative of the whole group or if we are dealing with an abnormal pattern of calcification. Although there is a considerable amount of variation in the spatial cytodifferentiation of dermal bones, Schmal- hausen (1968 p. 222), citing work by Lebedkina, reports the development of the nasal bones from two distinct centers of ossification in the primitive salamander genera Hynobius and Ranodon. Unfortu- nately, more specimens of B. adspersa at this stage

\),.

i

~~~~~~~i

Imm

FIG. Al. Ontogeny of nasal region dermal bones in Bolitoglossa adspersa. Stage 1. B. adspersa (MVZ 62965, both sides of the head). Nasals are ossifying from several centers of ossification.

a | Imm

b Imm

FIG. A2. Ontogeny of nasal region dermal bones in Bolitoglossa adspersa. Stage 2. a) B. adspersa (MVZ 143662). Prefrontal has just differentiated. b) B. adspersa (MVZ 143661). Slightly more developed stage in prefrontal ossification.

are not available. At S.V.L. of 19.7 mm (Fig. A2a), the ossification centers of the nasals are now com- pletely fused. The nasals grow predominantly antero-ventrally (see Fig. A2b for a slightly more developed stage). At this stage the nasal lies ventral to the foramen in the nasal capsule that allows for the passage of the terminal twigs of the medial branch of the N. ophthalmicus profundus V. This feature is not illustrated in Figure A2, but the foramina can be seen in several other figures, e.g., Figure 1. The number of nerve foramina in Bolitoglossa is variable, usually one or two closely located in the antero- lateral side of the nasal capsule, dorsal to the external naris (see Fig. 1). The nasals grow until they eventually cover a large portion of the nasal capsule. At the 19 mm stage (although initial ossification must occur between 16-18 mm S.V.L.), a tiny prefrontal is observed immediately posterior to the edge of the naso-lacrimal foramen. It is located medially with respect to the duct itself.

Later in development (Fig. A3, stage-24.8 mm



1mm

FIG. A3. Ontogeny of nasal region dermal bones in Bolitoglossa adspersa. Stage 3. B. adspersa (MIZ 143634, left side and detail of the right one). Devel- oping prefrontal has fused with the nasal.

2 .

Imm

FIG. A4. Adult condition in Bolitoglossa adspersa (MVZ 143645) with fused nasal and prefrontal bones.

.A4

1mm

FIG. A5. Adult condition in Bolitoglossa adspersa (MVZ 143655) with separated (unfused) nasal and prefrontal.

S.V.L.), the bones in the nasal region have enlarged considerably, but the cartilage of the nasal capsule still remains largely intact. The dorso-posterior edge of the nasal comes in contact with the antero-dorsal edge of the prefrontal above the naso-lacrimal foramen, and, in B. adspersa, they eventually fuse into a single element that wraps around the naso-lacrimal duct (Fig. A4).

However, in some specimens the fusion of the nasal and prefrontal never occurs and the generalized condition is observed (Fig. A5). In this condition, the breakdown of the cartilaginous matrix in the neigh- borhood of the prefrontal and posterior edge of the nasal is clearly seen. However, the naso-lacrimal foramen is always indicated by a cartilaginous ring.


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Issue Table of ContentsEvolution, Vol. 37, No. 5 (Sep., 1983) pp. 877-1100Front Matter [pp. ]The Heritability of External Morphology in Darwin's Ground Finches (Geospiza) on Isla Daphne Major, Galpagos[pp. 877-894]Quantitative Genetics of Development: Genetic Correlations Among Age-Specific Trait Values and the Evolution of Ontogeny [pp. 895-905]Morphological Variation in the Neotropical Salamander Genus Bolitoglossa [pp. 906-919]Continental Patterns of Morphological Variation in a South American Sparrow [pp. 920-930]Structural Relationships Between Spines and Lateral Plates in Threespine Stickleback (Gasterosteus aculeatus) [pp. 931-946]Breeding System, Genetic Variability, and Response to Selection in Plectritis (Valerianaceae) [pp. 947-956]Pollen-Pistil Relationships in the Polemoniceae [pp. 957-967]The Influence of Paleozoic Ovule and Cupule Morphologies on Wind Pollination [pp. 968-986]Sexual Selection in the Lovebug, Plecia Nearctica: The Role of Male Choice [pp. 987-992]The Evolution of Aposematic Coloration in Distasteful Prey: An Individual Selection Model [pp. 993-1000]A Comparison of Theoretical and Electrophoretic Assessments of Genetic Structure in Populations of the House Sparrow (Passer domesticus) [pp. 1001-1009]Genetic Differentiation Within Subdivided Populations of Formica Ants [pp. 1010-1022]Genetic Variation for Host Preference Within and Among Populations of Drosophila tripunctata [pp. 1023-1033]DNA/DNA Hybridization Studies of Muroid Rodents: Symmetry and Rates of Molecular Evolution [pp. 1034-1051]Larval Adaptations and Patterns of Brachiopod Diversity in Space and Time [pp. 1052-1061]The Role of Body Size in the Assembly of West Indian Bird Communities [pp. 1062-1074]Homage to Santa Anita: Thermal Sensitivity of Sprint Speed in Agamid Lizards [pp. 1075-1084]Notes and CommentsA Pitfall in Using Painted Insects in Studies of Protective Coloration [pp. 1085-1086]Costs of Thermoregulation in Adult Pinnipeds [pp. 1087-1091]Why Are Juveniles Smaller Than Their Parents? [pp. 1091-1094]

Book ReviewsBiology, Culture, and Punctuationism [pp. 1095-1096]Dealing with Creationism [pp. 1097-1100]

Back Matter [pp. ]

Akberch 1983 Morphological Variation in the Neotropical Salamander Genus Bolitoglossa

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Transcript of Akberch 1983 Morphological Variation in the Neotropical Salamander Genus Bolitoglossa