Vertebral numbers in male and female snakes: the roles of natural, sexual and fecundity selection R. SHINE School of Biological Sciences A08, University of Sydney, NSW 2006 Australia
Keywords:
Abstract
adaptation; comparative analysis; reptile; sexual dimorphism; snake.
The relative numbers of trunk (body) and caudal (tail) vertebrae in snakes might be in¯uenced by at least four processes: (1) natural selection for crawling speed, (2) fecundity selection for larger trunk size in females, (3) sexual selection for longer bodies or tails in males and/or (4) developmental constraints (if an increase in the number of body vertebrae requires a decrease in the number of tail vertebrae, or vice versa). These four hypotheses generate different predictions about the relationship between sex differences in the numbers of body vertebrae vs. tail vertebrae. I collated published data to test these predictions, both with raw data and using phylogenetically independent contrasts. Some snake lineages show a negative correlation between the magnitude of sex disparities in trunk vs. caudal vertebrae whereas other lineages show the reverse pattern, or no correlation. Thus, different selective pressures seem to have been important in different lineages. Vertebral numbers in snakes may offer a useful model system in which to explore the con¯icts between natural, fecundity and sexual selection.
Introduction Although many different processes can generate modi®cations to biological structures through time, Darwinian theory has generally stressed the role of selective forces (rather than drift, founder effects, etc.) in this respect. De®nitions of selective forces differ among authorities, but most evolutionary biologists would accept that one sensible way to classify types of selection would be with respect to the kinds of traits that are modi®ed. Thus, natural selection (sometimes called survival selection) favours the elaboration of traits that enhance an organism's probability of survival, fecundity selection favours traits that enhance reproductive output and sexual selection favours traits that enhance reproductive success in interactions with competitors or sexual partners (for discussion of such schemes, see Lack, 1968; Mayr, 1972; Arnold, 1983; Endler, 1986). Although there is strong evidence for all three types of selection listed above (e.g. Correspondence: Dr R. Shine, School of Biological Sciences A08, University of Sydney, NSW 2006 Australia. Tel.: +61 2 9351 3772; fax: +61 2 9351 5609; e-mail:
[email protected]
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Endler, 1983, 1986; Andersson, 1994), the potential interactions among them have attracted less attention. In many cases, the evolutionary trajectory of a single trait may be simultaneously affected by all three types of selection. For example, an increased body size in females might simultaneously increase the animal's probability of survival (e.g. by lower vulnerability to predation), her litter size and her attractiveness to males (Hawley & Aleksiuk, 1976; Calder, 1984; Hasegawa, 1990). In such cases, it may be dif®cult to partition the evolutionary pressures arising from these three different processes. The dif®culty is reduced in cases where the processes work in opposition. For example, the elaboration of extravagant male ornaments might be favoured by sexual selection but opposed by natural selection (Andersson, 1982). In such a situation, we can potentially measure the relative importance of each process, and interpret the overall balance (observed degree of trait elaboration) in terms of this con¯ict (e.g. Ryan et al., 1982). Clarifying such interactions among selective forces is dif®cult because complex interrelationships among traits raise the possibility of correlated responses to selection (Lande & Arnold, 1983; Lande, 1987). Also, natural
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selection is not the only determinant of phenotypic variation. Many traits are strongly in¯uenced by local environments as well as by genes, such that patterns of phenotypic traits may have little genetic underpinning (Seigel & Ford, 1991; Rhen & Lang, 1995). In other cases, traits may be determined genetically but be strongly in¯uenced by developmental constraints or by other nonadaptive processes such as founder effects, drift or phylogenetic inertia (e.g. Endler, 1986). Thus, we need to ®nd study systems that allow us to separate out such multiple in¯uences on evolutionary change. One approach is to select a system in which we can predict that different forces will generate mutually contradictory patterns. In practice, such predictions are often dif®cult to devise. In the present paper, I focus upon a system in which alternative selective forces (i.e. ignoring nonadaptive in¯uences on evolutionary change) may produce con¯icting optima. This system involves the relative numbers of vertebrae in the body vs. the tail in conspeci®c male and female snakes. Its advantages are as follows: 1 the morphological simplicity of snakes facilitates analysis of structural shifts (i.e. there are a limited number of ways in which one snake can differ from another); 2 by focusing on sexual dimorphism (i.e. comparing males and females within species), we avoid the confounding factors that inevitably complicate interspeci®c comparisons (Darwin, 1871); 3 the number of vertebrae in snakes is known to have a strong genetic basis (Arnold, 1988; Dohm & Garland, 1993); 4 in most snake species, vertebral numbers correspond to the numbers of scales under the body (ventrals) and under the tail (subcaudals) (Ruthven & Thompson, 1908; Gans & Taub, 1965; Alexander & Gans, 1966; Voris, 1975), traits commonly measured and reported for taxonomic purposes; and 5 because vertebral numbers are highly correlated with body and tail lengths, the balance between body vs. caudal vertebrae is likely to be in¯uenced by all three of the selective processes discussed above (see next section). Microevolutionary forces acting on vertebral numbers in snakes Natural selection. The relative numbers of the two vertebral types modify locomotor speed and growth rates of some snake species. That is, there is a disadvantage to animals with too many or too few tail vertebrae relative to the number of trunk vertebrae (Arnold, 1988; Arnold & Bennett, 1988) or tails that are too long or too short relative to body length (Jayne & Bennett, 1989). Locomotor speeds and growth rates may be under directional selection (e.g. Jayne & Bennett, 1990). Thus, stabilizing selection may act to maintain a consistent ratio of trunk to caudal vertebrae in both sexes in such taxa (Arnold & Bennett, 1988; Arnold, 1988).
Fecundity selection. Larger female snakes produce larger clutches, thereby favouring increased maternal body size (Fitch, 1970; Seigel & Ford, 1987; Shine, 1994). Body size in snakes is highly correlated with the number of trunk vertebrae (Klauber, 1956; Saint Girons, 1978; Lindell, 1994), and snakes with more trunk vertebrae may grow faster (Lindell et al., 1993). Thus, selection for enlargement of the female's body plausibly would involve an increase in the number of trunk vertebrae, and hence an increase in the ratio of trunk vertebrae to tail vertebrae in this sex. Sexual selection. Male snakes may bene®t from having longer tails than conspeci®c females. They need to accommodate the hemipenes within the tail, and a longer tail may also increase a male's ability in courtship or male±male rivalry (King, 1989; Luiselli, 1996). If longer tails require more caudal vertebrae, then this process should involve an increase in the numbers of tail vertebrae, and hence a decrease in the ratio of trunk vertebrae to tail vertebrae in males. In the minority of snake species in which rival males engage in physical combat for mating opportunities, selection for larger body size in males (e.g. Shine, 1994) might have the opposite effect on relative numbers of tail vs. trunk vertebrae. Thus, sexual selection on males could favour either an increase or a decrease in the numbers of trunk vertebrae relative to tail vertebrae. These putative evolutionary forces generate opposing predictions about patterns of sexual differences in vertebral numbers. Natural selection for an optimal trunk/ caudal vertebral ratio should generate a positive interspeci®c correlation between sex disparities in the numbers of body vertebrae vs. tail vertebrae. That is, if males within a species have more trunk vertebrae than conspeci®c females, then the males should also have more caudal vertebrae (to maintain the same ratio). In contrast, neither fecundity selection (on trunk vertebrae in females) nor sexual selection (on either trunk or caudal vertebrae in males) should generate any such correlation. We would expect the magnitude of the sex disparity in body vs. tail vertebrae to be unrelated to each other. That is, if males have many more caudal vertebrae, they are no more likely to have more (or less) trunk vertebrae than conspeci®c females. These predictions are modi®ed, however, by the possibility of con¯icts between two or more opposing selective forces. Fecundity selection suggests that females may bene®t from having longer bodies relative to tails, whereas sexual selection suggests that males may bene®t from the reverse situation. One developmental mechanism by which this dimorphism could arise would be a shift in the position of the vent (Boulenger, 1913). That is, an increase in male tail length could be achieved by a reduction in body length, or an increase in female body length could be achieved by a reduction in tail length. This hypothesis implies that there is some factor
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constraining increases in total vertebral number, and thus generating a tradeoff between its two components. Pope (1935) pointed out that Boulenger's hypothesis could not adequately explain all cases of sex differences in snake scalation, because the direction of sex disparity in trunk vertebrae does not correlate perfectly with the direction of sexual dimorphism in body length. Nonetheless, Boulenger's (1913) concept of some degree of tradeoff between trunk and caudal vertebral numbers remains plausible. Were this to occur, we predict a negative correlation between the sex disparity in trunk vertebrae and that in caudal vertebrae. That is, a species in which males greatly exceed females in the number of tail vertebrae should tend to have females greatly exceeding males in the number of trunk vertebrae. In summary, natural selection should tend to generate a positive correlation between sex disparities in vertebral numbers of the trunk vs. the tail. We would not expect any such correlation from either sexual selection or fecundity selection acting alone. If constraints on the total number of vertebrae are important (i.e. there is a limiting resource, and thus a tradeoff between sexual and fecundity selection), then we predict a negative correlation between sex disparities in the two vertebral types.
Materials and methods I collated published data on scale numbers and body sizes in snakes to test the predictions outlined above. Data were taken from Pope (1935), Kopstein (1941), de Silva (1969), Pitman (1974), Gloyd (1978), Ernst & Barbour (1989), Gloyd & Conant (1989), Degenhardt et al. (1996) and Rossman et al. (1996). In some cases data on more than one population was obtained for a single species. I used the mean scale count for each sex if that information was available, but otherwise took the midpoint of the range provided. These two measures are very highly correlated (Lindell, 1994). Snout±vent length (SVL) was used as the measure of body size. I used mean values for adult animals of each sex if those data were available, but otherwise relied on maximum size of adults of each sex. The degree of sexual size dimorphism in mean adult body size is highly correlated with that at maturation and at maximum size (Gibbons & Lovich, 1990; Shine, 1990). Thus, use of these approximations should introduce only minor error. Also, this error should be random with respect to the hypotheses of interest. Thus, it should not bias results from the analyses. To quantify sexual size dimorphism (SSD), I used the index proposed by Gibbons & Lovich (1990). This method involves dividing the mean SVL of the larger sex by that of the smaller sex, subtracting 1 from the result, and arbitrarily expressing the index as positive if females are the larger sex, negative if males are the larger sex. This index overcomes many of the statistical
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dif®culties associated with the use of conventional ratio measures (Gibbons & Lovich, 1990). Two types of statistical tests were carried out on the resulting data set. First, I treated each population as an independent unit, looking for general patterns in sexual dimorphism and scalation. I refer to these as `tips' analyses, because they use data on the tips of the phylogenetic tree. Second, I superimposed the data onto phylogenies of the lineages involved, to assess phylogenetic shifts in the characters of interest (using the program CAIC: Purvis & Rambaut, 1995). This technique avoids the problem that many patterns may be generated by phylogenetic inertia rather than functional relationships among variables (Felsenstein, 1985; Harvey & Pagel, 1991). Phylogenies used for these tests came from the papers and books listed above, plus recent syntheses by Thorpe et al. (1997) and Lee & Shine (1998). In the absence of reliable data on branch lengths, I assumed constant branch lengths in all analyses. Because the analyses identi®ed an anomalous pattern in New World natricines, I also X-rayed six specimens of a gartersnake species (Thamnophis sirtalis) to verify the assumption that scale counts correspond to vertebral numbers within this genus. These specimens came from a commercial biological-supply company, without locality data.
Results I obtained data on sex disparities in scale numbers for 315 populations of snakes (255 species), although in 45 of these cases I was unable to locate data on body sizes for both sexes. I did not include data on lineages (scolecophidians, hydrophiids) where previous studies have shown that vertebral numbers cannot be con®dently inferred from ventral scale counts (Alexander & Gans, 1966; Voris, 1975). The data were divided into six phylogenetic groups for analysis: six populations of aparallactines (®ve species), 150 non-natricine colubrids (135 species), 287 Old World natricines (22 species), 56 New World natricines (48 species), 10 elapids (eight species) and 66 viperids (37 species). The natricines were separated from other colubrids, and divided geographically, for two reasons. First, they are a speciose and well-studied group. Second, data on vertebral numbers suggest that New World natricines differ in important ways from the other snake taxa studied (see below); hence, it is of interest to examine patterns within this lineage as well as their close relatives from the Old World. Overall patterns The general situation in snakes (as represented by my data set) is as follows. Females generally exceed conspeci®c males in body size (SVL; true in 76% of samples) and, less markedly, in the number of trunk
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vertebrae (females greater in 190, fewer in 66, equal to males in 59). Thus, for species in which males and females differ in the number of trunk vertebrae, females have the larger number in 74% of cases (against a null expectation of 50%, v2 60.63, 1 d.f., P < 0.001). The reverse is true for tail vertebrae. Males exceed females in this respect in 252 species ( 94% of those with dimorphism), the reverse occurs in 17 cases and the two sexes were equal in 44 cases (against a null expectation of 50%, v2 205.30, 1 d.f., P < 0.001). Hence, female snakes generally grow larger than conspeci®c males, and have more trunk vertebrae but fewer caudal vertebrae. Overall, I obtained data for species with mean adult SVLs from 14 to 204 cm, with numbers of trunk vertebrae from 113 to 270 and tail vertebrae from 11 to 178. Males displayed 33 less to 18 more trunk vertebrae than conspeci®c females, and 7 less to 17 more tail vertebrae. Do vertebral numbers correlate with body and tail sizes in both sexes? First, I evaluated the assumption that vertebral numbers correlate with body size, because this is an important underpinning of the idea that selection on body size and tail size will affect the number of vertebrae. The correlation between SVL and vertebral number is very strong overall, using average values per species (Lindell, 1994). Nonetheless, it is worth checking that it is also true for the sexes when considered separately, and for tail length as well as body length. Most previous analyses have not separated data by sex (but see Saint Girons, 1978), and I am unaware of any previous analysis of tail length in this respect. My data con®rm that more scales correlate with a longer body (or tail). Snout±vent length vs. trunk vertebrae. In both males and females, vertebral number was positively correlated with snout±vent length (`tips' analysis: females n 268, r2 0.21, P < 0.001; males n 270, r2 0.22, P < 0.001). The same pattern was evident within each of the phylogenetic lineages, and was statistically signi®cant (P < 0.05) for both sexes within aparallactines, non-natricine colubrids and New World natricines. The independent contrasts test also yielded signi®cant positive correlations between changes in body size vs. changes in numbers of body vertebrae (n 126; for females, r2 0.33, P < 0.0001; for males, r2 0.35, P < 0.0001). That is, phylogenetic shifts in body size have been consistently accompanied by shifts in vertebral numbers. When lineages were tested separately, the regressions using independent contrasts were also statistically signi®cant for both sexes within the non-natricine colubrids and the New World natricines.
Tail length vs. caudal vertebrae. Data on mean tail lengths of males and females were analysed for two lineages for which detailed information on these topics was available: pit-vipers related to Agkistrodon (data from Gloyd & Conant, 1989) and New World gartersnakes (Thamnophis: data from Rossman et al., 1996). Within both groups, longer tails contained more caudal vertebrae (pit-vipers ± males n 33, r2 0.44, P < 0.0001, females n 32, r2 0.59, P < 0.0001; for gartersnakes ± males n 25, r2 0.51, P < 0.0001, females n 25, r2 0.76, P < 0.0001). This result was supported by the comparative analysis (pit-vipers ± males n 24, r2 0.38, P < 0.001, females n 24, r2 0.41, P < 0.001; for gartersnakes ± males n 21, r2 0.32, P < 0.007, females n 21, r2 0.50, P < 0.0003). In summary, both sexes show high interspeci®c correlations between mean adult length (of the body or the tail) and the number of vertebrae therein. When one of these variables changes during phylogeny, the other variable generally changes at the same time, in the same direction. Is the relationship between vertebral number and body length the same in both sexes? Another assumption of the hypotheses discussed above is that the relationship between body length and vertebral number is similar in conspeci®c males and females (although it may differ between species: Lindell, 1994). If this assumption is violated, selective forces could modify body proportions without in¯uencing vertebral numbers. The assumption is readily tested by A N C O V A , with sex as the factor, length of the body segment (either trunk or tail) as the covariate, and vertebral number as the dependent variable. Again, this assumption was broadly supported. Snout±vent length vs. trunk vertebrae. Conspeci®c males and females did not differ in the relationship between SVL and the number of ventral scales (slopes homogeneous F1,534 0.003, P 0.96; A N C O V A for effect of sex, F1,535 0.33, P 0.57; the same is true when the major lineages are tested separately). However, scatter within the regression for New World natricines was wide, and closer inspection showed that male and female gartersnakes (genus Thamnophis) differed signi®cantly in the relationship between body length and the number of trunk vertebrae. Males had more vertebrae per body length than did conspeci®c females (slopes homogeneous F1,40 0.79, P 0.38; A N C O V A for effect of sex, F1,41 6.75, P < 0.015). Comparative analysis on these data con®rms the general similarity between males and females in the relationship between SVL and trunk vertebrae. Changes in trunk vertebrae were consistently associated with concurrent changes in SVL (above), with the two sexes displaying similar relationships. This was true not only
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Sexual dimorphism in snakes
for the overall sample (slopes homogeneous F1,248 0.19, P 0.66; A N C O V A for effect of sex, F1,249 0.09, P 0.77) but also within the New World natricines only (slopes homogeneous F1,56 2.10, P 0.15; A N C O V A for effect of sex, F1,57 0.22, P 0.64) and within Thamnophis only (slopes homogeneous F1,26 1.79, P 0.19; A N C O V A for effect of sex, F1,27 0.30, P 0.59). Tail length vs. caudal vertebrae. Although the relationship between SVL and numbers of trunk vertebrae differed between the sexes within Thamnophis (in the tips but not the comparative analysis), the relationship between tail length and the number of caudal vertebrae did not. This result was true for comparative as well as tips analyses (tips shows slopes homogeneous F1,46 0.63, P 0.43; A N C O V A for effect of sex, F1,47 0.003, P 0.99, comparative shows slopes homogeneous F1,38 1.13, P 0.29; A N C O V A for effect of sex, F1,39 0.18, P 0.67). However, the sexes displayed a minor divergence in vertebral numbers relative to tail length in pit-vipers (Agkistrodon and related genera). The tips analysis revealed that vertebral number increased with tail length at similar rates in conspeci®c males and females (F1,61 1.05, P 0.31), but at any given tail length, males had more caudal vertebrae than females (F1,62 6.08, P < 0.02). Visual inspection of the data, however, revealed that the difference between the sexes was small (
