Skewed Sex Ratios in Snakes

RICHARD SHINE AND JAMES J. BULL

Fisher's sex ratio theory predicts that parents should contribute the sameeffort to raise sons as daughters over the population as a whole. Westudied sex ratios in the offspring of three live-bearing Australian snakespecies and reviewed published data on snake sex ratios at birth. Mostspecies produce young of each sex in equal numbers, but one elapidspecies which we studied, Notechis scutatus, produced a statistically sig-nificant excess of males (1.5:1). This imbalance is not consistent withFisher's theory. Two alternative models offer possible explanations, butthe data are not sufficiently comprehensive to test either model.

BIOLOGISTS have long been interested inthe ways natural selection can influence the

sex ratio (Darwin, 1874). Different age classeswithin a population may be characterized bydifferent sex ratios, but it is the primary sexratio (the sex ratio at conception) that will beacted upon by natural selection. Fisher (1930)proposed that natural selection favors equal in-vestment of effort by the parent(s) to the youngof each sex. This often, but not always, meansequal numbers of each sex at the end of paren-tal expenditure (Trivers and Willard, 1973).Fisher's principle has been discussed numeroustimes, and there is general agreement that histheorem is correct in the context of his assump-tions. The assumptions underlying Fisher's ar-gument may not always be acceptable, however,and Hamilton (1967) has discussed the conse-quences of removing some of these and hasshown that selection can favor unequal parentalinvestment between the young of each sex.

The subject of the evolution of sex ratios hasbeen of interest since Fisher (Shaw and Mohler,1953; Bodmer and Edwards, 1960; Kalmus andSmith, 1960; Verner, 1965; Hamilton, 1967,1972; Trivers and Willard, 1973; Leigh, 1970;Speith, 1974). Most of these works, however,present either special cases or redevelop Fisher'sprinciple that equal effort should be given tothe young of each sex. Fisher's treatment isquite brief and is difficult to follow. A few(MacArthur, 1965; Charnov, 1975; Eshel, 1975)have provided general cases for optimal sexratios. The large body of theoretical effortson sex ratio evolution has few sound data sup-porting it, aside from the general observationthat most organisms seem to produce the sexesin equal numbers. Hamilton (1967) has pre-sented convincing evidence that skewed sexratios in many parasitic invertebrates resultfrom selection in a system of inbreeding. Trivers

and Willard (1973) have proposed a model inwhich a female that biases her sex ratio will befavored provided that the population as awhole maintains equal effort.

We present sex ratio data obtained fromlitters of three species of elapid snakes andreview sex ratio data on snakes (at birth). Datafrom the literature suggest that most snakes havea sex ratio at birth of about 1: 1, although littersin one viperid and one crotalid may haveskewed sex ratios. One of the elapid specieswe studied produced significantly more malethan female offspring. This skewed sex ratiodoes not conform to Fisher's predictions. Twoalternative hypotheses are possible: these re-quire that the sex ratio genes are 1) sex-linked,or 2) locked into an autosomal linkage groupthat has a compensating advantage. Neitherhypothesis can be tested with the available data.

METHODS AND MATERIALS

We gathered data for sex ratios from littersof three live-bearing Australian species of theElapidae, Austrelaps superb us (copperhead),N otechis scutatus (tigersnake) and Pseudechisporphyriacus (red-bellied blacksnake). Althoughwe obtained gravid specimens over a wide geo-graphic area, most of our tigersnakes (Table 1)were collected from a small area (3 km2) nearUralla, N.S.W., and are thought to represent asingle population.

Gravid snakes were usually dissected within48 hrs of capture. Embryos were sexed by oneor both of the following methods: a) In latestages of development the hemipenes of themale are extruded from the body and wereeasily recognized; b) in early development achromosomal technique was used. These species(like all other advanced snakes) show well-dif.ferentiated sex chromosomes, the female being

228

SHINE AND BULL-SNAKE SEX RATIOS

11< HB ""ji I.'~ .. le ,11"

-,.. "It "'" ~!I!'

Notochis scutatus 2. =34

IIIW

,I ~0'61'1 1'1 I' 81&

... .. .. -.. ,. .. '" ..

Fig. 1. Karyotypes of (top) a male and (bottom)a female Notechis scutatus showing the sex chromo-some heteromorphism in the female (ZW).

heterogametic (ZW sex chromosomes), and themale, homogametic (ZZ sex chromosomes) (Fig.1). The W chromosome exhibits allocyclic be-havior, appearing as a condensed knob in inter-phase nuclei (Ray-Chaudhuri et aI., 1970). Wewere able to determine the sex of the embryoby observing cells stained in orcein: any snakein which each cell nucleus showed a singledark staining body (the condensed W chromo-some) was classified as a female, and any snakein which nuclei lacked this body was classifiedas a male.

It is unlikely that there is error in the sex

229

assignments. The two methods were comparedon 162 embryos and found to correspond inevery embryo. The nuclear sexing techniquewas compared with gonad morphology on 24adult or sub-adult snakes and, again, found toagree in all cases.

All but one statistical test of significancewere based on the chi-square distribution forthe total sample of embryos (one degree of free-dom) against the null hypothesis that thesample came from a population whose primarysex ratio was 1:l. A sex ratio was consideredsignificantly different from I: I when P ~ 0.05.

RESULTS

Austrelaps superbus.-Data £i'om the copperheadsuggest that the sex ratio is male-biased, butthe sample size is too small for significance.Therefore no conclusion can be drawn. Theproportions of males (and litter sizes) were .75(16), .42 (12), .58 (24), .70 (10) and .50 (10).

Pseudechis porphyriacus.- There was great vari-ation in sex ratios between different blacksnakelitters; the large variance may be a consequenceof the small litter size (x = 11.3). The mean sexratio for the total (49.8% males) does not differsignificantly from I: 1 (Table 2; Fig. 2). A sexratio not significantly different from 1: 1 also

TABLE 1. COLLECTION AND DISSECTION DATA FOR GRAVID URALLA TIGERSNAKES (N. scutatus)AND THEIR EMBRYOS.

Non-gravidEmbryos in clutch S-V length weight of

Snake Collection of mother mothernumber date r1' '? nonfert. % males (cm) (gm)

I 28-XI-73 15 8 0 65.2 84.1 2552 28-XI-73 15 13 1 53.6 82.6 2903 6-XII-73 10 4 2 71.4 72.8 1604 16-XII-73 II 9 1 55.0 77.6 2095 16-XII-73 25 12 0 67.6 94.3 3656 16-XII-73 15 9 7 62.5 77.3 2127 22-XII-73 15 2 10 88.2 81.0 2278 22-XII-73 14 7 9 66.7 80.0 2309 6-1-74 9 9 0 50.0 79.0 237

10 10-1-74 9 10 0 47.4 80.6 239II 10-1-74 14 8 0 63.6 87.2 25212 16-1-74 16 7 I 69.6 75.8 17613 1-11-74 12 9 1 57.1 72.3 15314 14-11-74 6 10 I 37.5 82.2 28115 9-III-74 6 7 1 46.1 65.7 140- - -

192 124

Mean sex ratios: of all embryos, 60.8 : of clutches. 60.1

230 COPEIA, 1977, NO. 2

"'Q)

,I 11 I III IIIIIUl40 50 60 70

A

L,-9020 30 8'0

:;::

I

u ~III I50

I

:.::;

'0 2J

Q).0E"

Z 32I

,

~50

% Moles in Litter

,JL!wlJ,

Fig. 2. Histogram of clutch sex ratios for A)Notechis scutatus from Uralla, N.S.W., B) N. scuta-ius from elsewhere in N.S.W., and C) PseudechisporPhyriacus from N.S.W. and Victoria. Data forA) are given in Table 1.

characterizes most other species studied (Table2).

Notechis scutatus.-Litter size (x = 21.7) washigher than that of blacksnakes, and most of thetigersnake litters favored males (Table 1; Fig.2). The sex ratio differed significantly from1:1 in the total sample (59% males, P < 0.01),and also, in the Uralla sample (61% males,P < 0.01). Our discussion is confined to theUralla snakes because only this sample is likelyto represent a single popul2ltion. The Urallasample was tested in another way to obtainmore information about the nature of theskewed sex ratio: the average sex ratio of the15 clutches (60.1% males) also differed signif-icantly from 1: 1 [t-test, P (50.6 < x < 69.6)>.99]. (The exclusion of snake 7 decreased themean slightly (59.2), but in each test, the sexratio was significantly different from 1:1 at theP < 0.02 level or better.)

The test over the lumped sample of embryosshows that the total effort in the local popula-tion is biased toward males. It is the bias inthe population's sex ratio (primary) that de-termines the strength of selection for 1:1. Thetest of the average clutch sex ratio demonstratesthat the frequency of mothers with litters favor-ing males is already high among the adults andthat the skewed sex ratio in our sample is nota bias from a few large clutches with skewedsex ratios.

Published sex ratio data for complete littersof snakes indicate that most snakes produceyoung of each sex in equal numbers (Table 2).Apart from the tigersnakes, the only significantdepartures from 1:1 are 1) Bitis arietans, with

B

40% males; however, only four clutches fromwidely-separated localities are avaiable, and itis not known how the young were sexed; and2) Agkistrodon contortrix-litters may be male-biased, but there may have been some error insex assignments (H. S. Fitch, pers. comm.).

DISCUSSION

c Interpreting Fisher's rule for reptiles.-In orderto determine what sex ratio is to be expectedfrom Fisher's rule, the concept of parentalexpenditure must be clarified for these reptiles.Fisher (1930) states: "Parental expenditure in-curred with respect to children of each sex shallbe equaL" His definition of parental expendi-ture is vague. "Expenditure" may be consideredas the resource (e.g., time or energy) whichlimits clutch size (probably energy in snakes).Although this resource, energy, may be gatheredover a long period of time and stored prior touse, we are only concerned with the time atwhich this energy is irreversibly committed tothe offspring. If parents expend their effortover a long period of time, then the sex ratiocould vary from one extreme to the other duringthis time without violating Fisher's rule (Fisher,1930; Trivers and Willard, 1973). The optimalsex ratio is not affected by a differential mor-tality between the sexes after the end of paren-tal investment.

Reptiles, unlike mammals, rarely expend theireffort as parents over the entire period of em-bryological development. In most reptiles, theenergetic expenditure (commitment) on off-spring occurs over a very short period-ovulation(followed by immediate albumin and egg-shelldeposition in some). Even in some live-bearing(ovoviviparous) species of reptiles, parental ex-penditure following ovulation is minor; theyoung are basically self-sufficient entities insidethe mother, requiring only gaseous exchangeand water transport throughout development.(Dry weights of full term Notechis embryos areabout one-third lower than those of oviducaloocytes, so it seems unlikely that much energyis transferred from the mother to the youngduring pregnancy.) Also, since reabsorption ofinfertile oocytes and abortive young is minor(Shine, 1975), there is no retrieval of yolk onceit leaves the ovary.

In most reptiles, parental expenditure beginsand ends at ovulation; Fisher's rule, therefore,

predicts that a 1: 1 sex ratio should characterizeovulation or the first subsequent stage at whichsex is determined (fertilization in male hetero-

SHINE AND BULL-SNAKE SEX RATIOS 231

TABLE 2. PUBLISHED SEX RATIO DATA FOR BROODS OF SNAKES. We have included only thQse data which

include more than 40 offspring and represent complete clutches (no capture data). * - P < 0.05, ** - P <0.01, *** - P < 0.001.

Family

Colubridae

Crotalidae

Elapidae

Viperidae

Species

Natrix taxispilotaRegina grahamiR. septemvittataStoreria dekayiS. occipito-maculataThamnoPhis butleriT. ordinoidesT. sauritus sauritusT. sirtalis concinnusT. s. parietalisT. s. sirtalis

Agkistrodon contortrixAgkistrodon contortrix

A. hairsA. PiscivorusSistrurus c. catenatus

Austrelaps superbusNotechis scutatus

Pseudechis porPhyriacus

Bitis arietans

Vipera asPisV. berus

Natalsexratio

(% males)

4251494646535550605652

5775(?)***

464952

6059**50

40*5251

Numberof young

III87

128205

6144475067

121360

68238

6948

207

72499192

15511779

Numberof clutches

46579

20

1649

52317

42010

Authority

3 Franklin (1944)Hall (1969)Branson & Baker (1974)Clausen (1936)Blanchard (1937)Carpenter (1952)Stewart (1968)Carpenter (1952)Stewart (1968)Fitch (1965)Carpenter (1952)

Gloyd (1933)Fitch (1960, 1961)

(see text)Fukada (1962)Burkett (1966)Keenlyne and Beer (1973)

1014

148?

present studypresent study.present study

Pitman (1974)Naulleau (1973)Prestt (1971)

gametic systems). The data from Notechis scuta-ius appear to contradict this expectation.

The scant data from snakes suggest that N.scutatus is somewhat unique in having skewedsex ratios. Most snakes conform to the predic-tions of Fisher. This contradiction may not bereal, however, if any of the following three con-ditions obtain: I) differential size of Z and Woocytes, 2) differential fertilization capacity ofZ and W oocytes, 3) differential zygote survival.Data from dissections bear on each of thesepoints. 1) If more males than females are pro-duced, then an equal expenditure of effort couldstill be maintained if the average expenditure permale was less than that per female. This wouldrequire a difference in the energy (yolk) contentof the Z versus the W oocytes. We observedno such differences in sizes of oocytes or de-veloping embryos. In a sample of 10 male and12 female newborn N. scutatus from two litters,there was no significant difference betweenthe sexes in body weight at birth. 2) If thetigersnakes in our samples all produced equal

numbers of Z and W oocytes, then our male-biased results could be explained by a consis-tent failure of W oocytes to become fertilized.On this basis one would expect a correlationbetween male biasing and the number of un-fertilized oocytes in a litter. This is clearly notthe case for tigersnakes (Table 1); althoughthree snakes did show a high incidence of non-fertilization, there was no trend with the other12. 3) An early differential mortality betweenmale and female zygotes would have the sameeffect of biasing our data as W infertility, sinceit is difficult to distinguish between abortivezygotes and non-fertilized oocytes. This possi-bility is discounted for the reasons listed above.A differential mortality late in developmentcould not reconcile our results with Fisher's

model: the heterochromatin sexing techniqueis easily applied to abortive embryos and thesewere included in the data (only three cases).Thus, the skewed sex ratio in tigersnakes appear'to contradict Fisher's rule.

232 COPEIA, 1977, NO. 2

Alternative models.-There are several assump-tions in Fisher's model. Removing anyoneassumption gives rise to a new model in whichselection may favor the biased sex ratio. Theseassumptions include the following:

1) Autosomal genic inheritance. The Fishermodel describes selection acting to maximize theprobability of finding a parent's autosomalgenes in grandchildren but does not considerselection for genes on the sex chromosomes(Hamilton, 1967). If a sex-linked mutant arisesthat distorts sex ratio in its favor, then thetrait will spread because it leaves more of itsdescendants than the alternative alleles (whichdo not distort sex ratio) leave of their descen-dants (Shaw, 1958).

If the female is the heterogametic sex (as insnakes), females possessing this sex-linked mu-tant will produce clutches with biased sex ratios.If the mutant is on the Z chromosome then itwill be favored if it biases the offspring sexratio toward males; if W-linked, the sex ratiobias must be toward females. Selection willfavor such a mutant until the alternatives inthe population have been replaced. The popu-lation sex ratio at any time will depend uponthe frequency of the mutant gene and the ex-tent to which it biases sex ratio in each litter.However, such sex-linked mutants need notcause a permanent bias in the population sexratio: autosomal genes are favored if they sup-press the sex-linked sex ratio mutant (Hamil-ton, 1967; Eshel, 1975).

It is difficult to test the hypothesis that aZ-linked gene is responsible for the skewed sexratio in tigersnakes. Two critical postulatesmust be confirmed: a) females possessing themutant produce more male than female off-spring throughout their lives; and b) the mutantis passed from mother to son to granddaughter.

The available data are not sufficient to testthese ideas.

2) Affects only sex ratio. Fisher's model pre-dicts the optimal sex ratio. If a gene or a fullylinked combination of genes affects more thanjust sex ratio, then the fitness of the sex ratiogene will be partly determined by the othereffects. A very slight compensating increase infitness would negate the disadvantages of the1.5:1 sex ratio (Speith, 1974). Thus, a linkageof the sex ratio gene to other genes could ac-count for the skewed sex ratio in tigersnakes.

This hypothesis requires that: a) the mutantis inherited in an autosomal or W-linked man-

ner, and b) that some additional, beneficialeffect (to the gene or to the individual) assorts

with the mutant. Again, data to test thesehypotheses are not available.

3) Random breeding. Another of Fisher'sassumptions is that breeding is random. Hamil-ton (1967) has demonstrated that there is strongselection for skewed sex ratios when inbreedingis frequent (competition between males is re-duced) but such sex ratios always favor females.This example in snakes favors males.

4) Individual optimum. One could postulateadvantages to a male-biased population sex ratioon the basis of group selection. In view of theimprobability of group selection operatingunder most natural circumstances (Williams,1966), group selection does not seem to be alikely explanation for skewed sex ratios.

5) Constant fitnesses. The Fisher model dealswith constant average fitnesses. If fitness varies,then selection may favor parental ability to varythe sex ratio, but the population as a wholemust balance at 1:1 (equal effort). Trivers andWillard (1973) postulated for mammals that amale which was unusually fit at birth would belikely to retain this advantage throughout hislife, and thus to have a much greater reproduc-tive success (mating with many females) thanan average male; an unusually fit female wouldnot enjoy as great a reproductive advantageover an average female. The opposite wouldhold for young in poor condition at birth.Therefore, selection should favor a mother ingood condition (who is likely to produce fityoung) to produce males; the reverse is truefor a mother in poor condition.

It is difficult to interpret this theory forreptiles. One problem is that a female's repro-ductive potential (clutch size) is proportionalto her size; therefore, an unusually fit femalereptile might have as great a reproductive ad-vantage as an unusually fit male. If so, then amother in good condition which was likely toproduce fit young would not gain anything byproducing an excess of one sex. (The variancein male reproductive success might differ be-tween species, depending on the importance ofmale-male aggression.) We tried testing for arelationship between clutch sex ratio and physi-cal condition of the mother (wtj InS) but foundno consistent trend. Also, most reptiles producemany young per brood; they might vary thenumber of offspring rather than the fitness ofeach. Even if fitness varies, Trivers and Willardsuggest that the deviations on both sides of1:1 must cancel. This is not the case with thesnakes. However, there is some doubt that the

SHINE AND BULL-SNAKE SEX RATIOS

population does balance at equal effort in thesemodels (E. L. Charnov, pers. comm.).

These alternatives to Fisher's model include

only two plausible hypotheses to explain thetigersnake data. In both hypotheses the favoredsex ratio deviates from the female's optimum,either because the sex ratio genes are sex-linked,or because they are locked into an autosomal(or Wo) linkage group that confers a compensat-ing advantage. Under either model the skewedsex ratio should be temporary because of auto-somal selection moving the sex ratio closer to1: 1 (Eshel, 1975). Thus, the scarcity of skewedsex ratios in snakes is consistent with the transi-

tory nature of either of the suggested phenom-ena. Unfortunately, the available data do notpermit a rigorous test of either model; such testsmust come from long-term studies that deter-mine 1) the hereditability of the tendency toproduce skewed sex ratios, and 2) seasonalvariations in a female's clutch sex ratio.

It must be stressed that sex ratio selection at

the individual level is still poorly known. Theremay be wide variations in optimum sex ratiosbetween individuals of the same population(Trivers and Willard, 1973), and unless thesevariations are understood it is difficult to in-

terpret cases in which entire populations showskewed sex ratios. In future work we intend

to focus on sex ratio variation within popula-tions which balance at 1: 1, as well as examiningpopulations with skewed sex ratios.

ACKNOWLEDGMENTS

This study was conducted while JJB ac-companied J. M. Legler to Australia. We thankJ. M. Legler and H. Heatwole for assistanceand encouragement in the project. Support forJJB in Australia was received from Univ. ofUtah and an NSF predoctoral fellowship. JohnCann, Ken Slater and C. J. Parmenter providedus with some of the specimens used in this study.We thank the following for offering suggestionson the manuscript: M. C. Rechsteiner, J. H.Brown, D. Wiens, W. S. Parker and J. F. Berry,Univ. of Utah; H. S. Fitch, U. of Kansas; J.Basten, U. of Sydney. We are greatly indebtedto E. L. Charnov for his discussion on the ms.

and on sex ratio theory. We thank M. Vaughanfor typing. J. M. Legler was responsible forour initial interest in sex ratios.

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DEPARTMENT OF ZOOLOGY, UNIVERSITY OF NEW

ENGLAND, ARMIDALE, NSW AUSTRALIA 2351

AND DEPARTMENT OF BIOLOGY, UNIVERSITY OF

UTAH, SALT LAKE CITY, UTAH 84112 [also

Present Address (RS).]. Accepted 9 April1976.