the Board promulgates a policy which career of federal service-is obviously are made to really strengthen the Na-

it thinks is in the best interests of the subject to administrativediscipline. But tional Science Board, we are likely to
country, should approval be obtained does the same reasoning apply to Board witness a gradual shift of the control
from the Executive Branch before such members? In fact, the question of giv- of national science policies and pro-
a policy is announced? ing testimony before a congressional grams from the scientific community
Some Board members object to the committee itself has been raised. Must to the bureaucracy-with a consequent
constraints of this sort of administra- Board members offer only "approved" weakening and distortion of the whole
tive discipline, and at least in the past testimony? If so, this would seem to scientific effort.
have felt that prior approval of this seriously weaken the Board's voice in Reference and Note
type should not be required. It might terms of the purposes for which it was 1. V. Bush, Science-The Endless Frontier, 1945,
be reasoned that the director-who is a established. In my opinion, the nation reprinted by the National Science Foundation,
Washington, D.C. (1960).
presidential appointee, who is on the would best be served by making that 2. I have commented more fully on this matter
federal payroll, and who is making a voice stronger. Unless some provisions in my letter to Science 155, 1489 (1967).

selection by selecting the extreme op-

posite to the current sex ratio of the
population-that is, by producing a
Extraordinary Sex Ratios unisexual progeny of whichever sex was
currently in the minority. This game-
like feature, which has already led one
writer (3) to refer to genetically deter-
A sex-ratio theory for sex linkage and inbreeding
mined sex ratios as "strategies,"in the
has new implications in cytogenetics and entomology. sense of a play by the individual
against the population, becomes ac-
centuated as we proceed into circum-
W. D. Hamilton stances of local competition.
Before considering local competition,
however, it is convenient to discuss
the consequences of failure of some
The two sexes are usually produced out. Therefore 1:1 is the equilibrium of the genetic assumptions latent in
in approximately equal numbers. Fish- ratio. Fisher's argument.
er (1) was the first to explain why, The argument is not affected by the
under natural selection, this should be occurrence or nonoccurrence of polyg-
so, irrespective of the particular mech- amy, or by any differential mortality Sex-LinkedDrive underRandom Mating
anism of sex determination. His rather of the sexes, provided this is uncorre-
tersely expressed argument has been lated with the sex-ratio genotypes. Fisher's argument does apply to all
clarified by .subsequentwriters (2) and More precisely, what has been called cases where sex-ratio control is by
seems to be widely accepted. In bare "Fisher's principle" of the sex ratio genes acting in the homogametic sex,
outline, the factor of parental care be- states that the sex ratio is in equilibrium or in the female under the male-hap-
ing ignored, it may be given as fol- when, in the population as a whole, the loid system [contrary to some earlier
lows: totals of effort spent producing the two statements of mine (4)], or by genes
1) Suppose male births are less com- sexes are equal. If the totals are not on the autosomes acting in the hetero-
mon than female. equal, producers of the sex correspond- gametic sex. In all these cases the total
2) A newborn male then has better ing to the lesser total have an ad- number of the gene-bearer's grandchil-
mating prospects than a newborn fe- vantage. dren is a true measure of the propaga-
male, and therefore can expect to have This article is concerned with situa- tion of the gene. This is not so in the
more offspring. tions where certain underlying assump- case of sex-linked genes acting in the
3) Therefore parents genetically dis- tions of Fisher's argument do not hold. heterogametic sex.
posed to produce males tend to have It will be seen that such situations For simplicity of argument, suppose
more than average numbers of grand- must be quite widespread in nature. the male is heterogametic. Then grand-
childrenborn to them. As regards ecological assumptions, for children through daughtersare obvious-
4) Therefore the genes for male-pro- example, Fisher's argument is restricted ly irrelevant to the fitness of a gene
ducing tendencies spread, and male to the actually unusual case of popula- on the Y chromosome. This fitness is
births become commoner. tion-wide competition for mates. A con- measurable entirely by the number of
5) As the 1:1 sex ratio is approached, trary case wherein the competition is sons. Sex-ratio control in the male is
the advantage associated with produc- local is discussed in some detail. In effectively the same as genetic control
ing males dies away. some features it has an unexpectedly over the relative success of the X-bear-
6) The same reasoning holds if fe- close similarityto certain types of situa- ing and Y-bearing sperm in fertiliza-
males are substitutedfor males through- tions considered in the "theory of tion. Suppose the Y chromosome has
The author is lecturer in genetics in the depart-
games." Already the above outline mutated in a way which causes it al-
ment of zoology and applied entomology, Imperial seems to show that an individual sup- ways to win in the race to fertilize.
College, University of London, working at Im-
perial College Field Station, Silwood Park, Sun- posedly able to choose the sexes of A male with the Y mutant then pro-
ninghill, Berkshire, England. offspring would do best under natural duces nothing but sons. Provided these
28 APRIL 1967 477
sons, who also carry the mutant, can- female has chanced to mate with a differential X chromosome occasions a
not be in any way discriminatedagainst male carryingthe mutant. similar theoretical disaster but brings
in the unrestricted competition for Figure la represents such an epi- it about much more slowly. This is
mates (a situation which is implied if sode, in which the starting condition partly because in this case selection is
mating is random for the whole popula- is one mutant-bearing male in 1000 intrinsically slower. Unlike the Y, the
tion), the Y mutant will have a con- males. On the basis of the admittedly mutated X chromosome is not exposed
stant selective advantage.As the mutant severe assumptionthat females produce to selection in every generation, and,
spreads, the population sex ratio will only two offspring each, it was found overall, as might be expected from the
become more and more male-biased that in the 15th generation the ex- proportion of its generations that an
and the population itself will become pected number of females is less than ordinary X chromosome spends in
smaller and smaller; finally the popula- one. males, its spread is about one-third as
tion will be extinguished, after the last A similar extreme mutation on the fast. In Fig. 2 the two types of tran-
sience are compared, and the tran-
sience of an autosomal gene causing
fully effective meiotic or gametic drive
is also shown. As might be expected,
the speed of the autosomal gene is
intermediate. The progress toward ex-
tinction due to a driving X mutant is
delayed by the occurrence of polygamy.
(a) Spreo Indeed, so long as the males remain
sufficientlynumerous to fertilize all the
females, the population should show
acceleratingexpansion (Fig. lb).
1000 Cases of X-linked "drive" are not
uncommon in wild populations of some
species of Drosophila, and their poten-
tial threat to the species has been rec-
ognized (5). Cases of autosomal drive
have been under study and discussion
for some time (6). With perhaps one
exception, mentioned below, no equal-
ly striking cases of Y-linked drive have
* 9000o
been reported. Perhaps, in view of the
u general inertness of the Y chromosome,
this is not surprising. It is surprising,
XX however, that the exceptional latent
M amXY, L? ^\sV^} \/\f I danger to the species presented by this
form of drive has received so little
comment; I suggest (and to the best of
my knowledge this is the first time the
suggestion has been made) that it may
help to explain why the Y chromosome
is so often inert. A population in which
a driving Y mutant was spreading
could be saved by another mutation,

Fig. 1. Populationand its distributionby

sex and genotype in the course of na-
tural selection of (a) a Y chromosome
and (b) an X chromosome, having com-
plete drive in spermatogenesis. Mating is
random,and normalmalesgive a sex ratio
of ?2. It is assumed (i) that mated females
Hhavetwo offspring each, so that, before
mutation produces the driving chromo-
_some, the population is stationary, and
(ii) that males can fertilize only two
1females each, so that, in (b), from the
first generation in which the sex ratio is
less than 13 (generation 27), some females
have no offspring because they are un-
mated. Both populations start with one
chromosomeof the driving type in 1000
chromosomes. Extinction is considered to
3035
occur after the first generationin which
0 5 10 15 20 25 40 the expected number of females is less
Generations than one.
478 SCIENCE, VOL. 156
on an autosome or on the X chromo- The fact that no other case like that in wild populations of Drosophila is
some, which was capable of inactivat- of Aedes aegypti has yet been reported, not very surprising, although, in order
ing the relevant region of the Y in contrast to several cases of X-linked properly to understand their existence
mutant. That such a mutation would drive, accords with the drastic rapidity in a permanent polymorphism, there
spread follows from Fisher's principle. of spread of the driving Y mutant and has to be postulated either a severe
In doing so it would slow down (al- its immediately adverse effect on re- disadvantage to females homozygous
though it would never arrest) the productive potential. Presumably an for the driving chromosome (9) or
spread of the Y mutant and, at the outbreeding species cannot long con- some basis of interpopulation competi-
same time, would cover up its effect. tinue to exist if it has a Y chromosome tion, as Novitski (5) suggested and as
It seems probable that something like likely to mutate in this way. The same is shown in the model given below.
this has happened in the mosquito does not apply if the female is heter- Altogether, the evidence for the
Aedes aegypti, if the genetic situation ogametic. An extreme sex-ratio swing workability of the suggested differen-
inferred by Hickey and Craig (7) is which is very suggestive of the spread tial evolution of the Y chromosome is
correct. In this case the "Y" is ap- of a driving Y chromosome has recent- good. There is evidence that genes and
parently a male-determining gene, cer- ly been reported in a butterfly popula- other chromosomes can suppress the
tainly not a whole chromosome, and tion (8). As with the driving X chro- "sex ratio" trait in Drosophila (10), that
it seems that, in the strains where the mosome under male heterogamety, heteropycnosis may be a cytological
driving Y mutant exists, there may be such an event would be advantageous manifestation of such inactivation (11),
several different "X" alleles which re- to the population at first. The frequent and that heteropycnotic regions some-
strain the action of the Y mutant in discovery of driving X chromosomes times do cause disturbed segregations
differing degrees. It is hybrid males
from outcrosses of such strains that of-
ten give extreme male-biased sex ratios.
All-male progenies we,re sometimes re-
corded. 0

Hickey and Craig have pointed out .

the potentiality of their effect for bio-
logical control. They did not attempt
to demonstrate the capability for spread .99 p
0
of their driving Y gene but did show
in some experiments that it could main- .98
0
tain itself at high frequency, with .97 0
0
consequent detriment to the experimen- .96 0
tal population. Some other experiments t .95 0
A' 0
showed, however, a rapid masking of
L) 0
the sex-ratio effect. This may have .90
0
.
0
U
been due to reconstitution of the re- -,V
Un 0
straining mechanism which operated in CT) .0o L 0
the paternal population. Clearly, if the 0 0
0
view presented here is valid, a princi- .70
>,
ple of application in biological control U .60 0
will involve repeated backcros!sing of 50
0
the hybrid male-producing males to fe-
?) .40 10 20 * 30 40 50 60
males of the susceptible population. L. 0 * 0
. 30 0
Unless this is done prior to liberation
0
Generation
of male-producing males, some part of
the genetic mechanism on other chro-
0 I- 0

mosomes which previously masked the E

E
sex-ratio effect (for example, a reces- 0L. ..lo
0 0
sive gene) is likely to be introduced
C) _)
at the same time. It should be worth- .05 0
.04
0 *
while to look for male-producing effects .03
in racially hybrid males in other out- 00
.02 * 0
breeding species with male heterogame- 0
ty, and also perhaps for genetical de-
.01
vices by which the Y chromosome
0.0
could be freed from the inhibitory ac-
0
0
tion of the rest of the genome. The
0
implied method of biological control
is in theory very powerful, since the .0

mere seeding of a population with a *?

few prepared males could cause its ex- .001
10

termination or at least its reduction

Fig. 2. Logistic plots showing the progress in frequency of occurrence of sex chromo-
to a density where mating was no long- somes (X', Y') and an autosome (A') having complete drive in spermatogenesis. Each
er effectively random. course starts with one chromosome of the mutated type in 1000 chromosomes.
28 APRIL 1967 479
(12). In general it is gametogenesis by normal immigrants from surround- This may be called the Y-chromo-
rather than fertilization that is the like- ing areas. Thus some sort of equilibrium some fitness in such a female in such a
ly arena of the dysgenic effects that could occur. group. It is required to know whether
have been considered. Hickey and Craig Another biological situation in which the average for type a, taken over all
show that their effect is probably due the spread of the aggressive Y mutant such sets, is above or below the whole-
to events that either suppress produc- is eventually checked is as follows. population average for Y-chromosome
tion of X-bearing sperm or cause such Free-moving females search for iso- fitnesses. This will indicate whether the
sperm to degenerate, and McCloskey lated food objects, or "hosts." Each Ya chromosome is gaining or losing in
(13) has recently emphasized the ex- host is colonized by a certain number frequency.
treme scarcity of evidence of gene ac- and is eventually exhausted through Consider therefore the n-1 associates
tivity in animal gametes in general. feeding of the progenies. The subpopu- of a type-a female selected at random
However, McCloskey admitted that his lation of adults reared on a host mates from the whole set of those that have
experiments with Drosophila could randomly within itself; no males suc- succeeded in finding hosts. Let F,. rep-
not exclude the possibility, significant cessfully mate outside their own group. resent the probability distribution of the
for the present hypothesis, that genes Inseminated females emigrate to take number (r-1) of type-a females among
in the main heterochromatic regions part in population-wide competition to these associates. The average ya_
might be active in the sperm, and he discover new hosts. In this system, chromosome fitness, W,, is then seen to
also noted some hints that mammalian matings will be a mixture of sibmatings be
sperm may not be so inert genetically and outcrosses, the former becoming
n
as the sperm of Drosophila. Therefore, common when the number of females
Wa = Fr-2(1 - Xr)
just possibly the indications of high settling on a host is small. It is at 1 r
primary sex ratios in some mammals once obvious that the driving Y mutant
(14), and of higher activity of Y-bear- cannot supervene completely in such The general average for Y-chromo-
ing sperm in rabbits and cattle (15), a population, provided the population some fitness must be
are relevant evidence of a stronger is large and the females are fecund,
W = 1-X
tendency of the Y chromosome to for the grouping sets a limit to the
evolve spermatic drive. Somewhat extent to which a female's brothers where X is the sex ratio of the whole
against this possibility, however, is the can be outnumbered by the mutants population. Explicitly,
evidence, for plants (in which gene ac- among her suitors, and there always
tivity in the penetrating pollen tubes remains a finite chance that she will X = px. + (1 - p)Xb
is well known), that it is the X-bearing mate with a brother.
where p is the frequency of ya.
pollen that tends to win under com- To facilitate further analysis of such
petitive conditions (16). This is under- a situation, let us suppose that always The selective advantage, Ea, of the
Ya chromosome with respect to the
standable on the basis of Fisherian exactly n females settle on a host and
theory only if it is the genotype of the that the progenies reared are equal. population average is
style that controls the race, for, as Suppose that there exist two types of n
Lewis has pointed out, abundant pol- Y chromosome, ya and Yb. EaF Wa --
Fy- W x-(=F1 )
lination will usually imply that males Females accept only one insemina-
are common in the neighborhood, so tion, so the host-seeking females will
that to favor the production of females be of two types, according to the con- = F + (1 - P)(xb- x.) - 1. (1)
is the correct policy. With occasional 1
tents of their spermathecae: XYa-
pollination the sex ratio produced tends bearing and XYb-bearing, or, more Differentiating, we obtain
to be 1:1. This is, no doubt, the sex briefly, type-a and type-b. Suppose
ratio of the pollen grains, but that a these two types are constrained to give dEa _ 1 Fn r)r xi - (1
male-biased ratio is not in some way progenies in which males form frac- dx
--~ n 1 --F
xa n~ Xr p).
brought about from sparse pollination tionis xa and xb of the totals. Such
may be partly due to the factor of fractions are convenient measures of When x: Xb= c, this reduces to
local competition, now to be consid- the sex ratio, and hereafter in this
ered. article all sex ratios are given in this Fr (n - r) -(1-p),
form.
Consider the set of hosts which hap- which is zero only when
Sex-Linked Drive with pen to be shared by r type-a females
Local Competition for Mates and by n-r type-b females. The sex
ratio, X., in the progeny of this set n- - Fr'
In a "viscous" population-that c =1 .(2)
is will be
to say, one where the individual can n(l -p)
Xr = [rxa + (n - i)Xb]/n Now consider the simple and plausi-
mate only with a rather permanent set
of neighbors who tend also to be his Through fair competition for mates, ble case where the settling on hosts
relatives-it is clear that the initial a particular type-a female may be ex- is random. The distribution of r will
spread of a driving Y mutant from pected to be responsible for the be binomial and so will be the distribu-
the point where the mutation occurred spermathecal contents of a number of tion of the number of a-type associates
will bring about a local collapse of emigrant females proportional to of the randomly selected a-type female:
population due to the lack of females,
and vacant space will tend to be filled x-
Xr
(1 - X.) Fr-=
(=
156
- p)'(SE pO-
S
1
480 SCIENCE, VOL. 156
Then Non-Sex-Linked Control with to the Fisherian case and, corre-
n Local Competition for Mates spondingly, the formula shows the un-
Frr (n - )p+ 1 beatable ratio ten,ding to applroach /2.
1 Apart from the supposition of ex-
s< At the other extreme, the case
linked control, the above model cc)n- n = 1 obviously corresponds to a sys-
and Eq. 2 becomes travenes Fisher's tacit assumption of t in- tem of completely sibmated lines. That
restricted competition for mates. It is the theoretical equilibrium ratio is then
c = (n - l)/n. (3)
interesting, therefore, to consider wlhat zero merely implies that a female's
I am satisfied, although I have not this same model situation implies whien advantage depends wholly on the num-
strictly proved, that this is indeed the this is the only assumption broken - ber of fertile emigrant females she can
only "unbeatable" sex ratio for the situ- that is, when control of sex ratio is of produce from her host. It is not in her
ation: the Y chromosome that pro- one of the kinds which has been notLed interest to produce more males than are
duces it has a selective advantage over to give the relatiolnships of Fishe.r's necessary to ensure the fertilization of
any other, whatever the current gene principle under the condition of p;an- all her daughters.
frequency. mixia. The model breeding structiare
The above model equilibria do not forces sons into competition with c ene
seem very realistic. Species in which another, so that although there may be, A Biofacies of Extreme
the sex ratio comes to be controlled in general, a shortage of males, p ro-
Inbreeding and Arrhenotoky
by Y-linked drive probably become duction of males does not necessar:ily
quickly extinct even if they are pro- pay off in terms of grandchildrnen: Among small anthropods, wherever
tected to some extent by grouping of whether it does so depends on the ,sex reproduction is quite regularly by
the sort described. Unfortunately no ratios of offspring produced by otlher brother-sister mating there seems to be
general analysis of the less drastic situa- females of the group. extreme economy in the production of
tion in which there is gametic drive by An approximate analysis can foil ow males, as predicted. Most of the cases
the X chromosome has been achieved. the lines of the foregoing analysis v(ery which have been noted are listed in
However, deterministic computer simu- closely, provided it is supposed tlhat Table 1.
lation of the population genetics for there are only two types of femrlie, It is probable that all of them re-
n = 2 shows that the "unbeatable" A and B, and that produce by arrhenotoky-that is, by the
ratio is between 0.070 and 0.072. This process in which males are derived al-
fitness cc N of inseminations by sons
result must also hold if control of the N of daughters. () ways, and only, from unfertilized eggs.
sex ratio depends on the genotype of This process has been found to be
the male in male haploid species. Such Obviously such a simple scheme c.an- associated with haploidy of the males
control is certainly unusual, but it not give a proper genetical represen ta- in all cases that have been investigated
seems to occur in the eulophid Dahl- tion of a situation, but, as mentior led cytologically; therefore, male haploidy
bominus fuscipennis (17). This is an below, it has been found to give a f air is a strong supposition for most of the
inbreeding species, and its sex ratio, correspondence to the genetical mo del cases in Table 1. However, with a few
about 0.09, is of the order expected. for n = 2, while, for the panmic:tic species not only is there no direct
But the case is peculiar, and the under- case, it has already been accepited evidence that males are usually im-
lying theory still has a major gap in in the literature (19). paternate but also there is none that
that it is not known whether the "un- Using these assumptions and obvi(3us female-to-female parthenogenesis (the-
beatable" sex ratio for n = 3 is above developments of our notation, we hav e lytoky) does not occur. But in view of
or below 0.07. In view of the possible the general conformity of such cases
n
relevance to the X-linked sex-ratio ef- - (for example, the fig insect and the
WA.. (1 - r.) (1 - XA)
fects in Drosophila, this point deserves Fr_ + moth ear mite) with the others, and of
1 X}
further study. what is known of related species, it
Although male-haploid inheritance is Since we are now concerned with the will be surprising if they turn out to be
idenltical to the sex-linked type, from production of daughters as well as of not normally arrhenotokous.
the point of view of sex ratios a dif- sons, the mean fitness in the popt ila- Taken together, the data suggest the
ference enters if the males fail to fer- tion must be taken as 2(1 - X). outline of an ideal extreme biofacies
tilize all the females. This difference is Therefore which may be described as follows:
due to the ability of the females, in 1) The primary sex ratio is
cases of male haploidy, to produce all- n
XA spanandrous-that is, females greatly
male broods parthenogenetically. With EA - Fr- X + 2(1 - p)(XB - x) - 1.
1 preponderate.
sex ratios as extreme as those just 2) Reproduction is arrhenotokous.
mentioned, such failure of polygamy The foregoing equation is the saLme 3) There is at least one male in
would not be surpising. In the case of as Eq. 1 except for the factor 2 in every batch of offspring.
random mating it is known to intro- the second term. Hence, by just the 4) There is gregarious development,
duce a tendency toward unstable alter- same argument we can arrive at the as a group of siblings, from egg to
nation of sex ratios which is quick- unbeatable sex ratio adult.
ly disastrous if the mated females are 5) Adult males eclose first and can
being forced to produce only female (n - 1)/2n () mate many times.
offspring (18). From this aspect, also, for the case of random association. 6) Mating takes place immediately
the breeding structure of the model As type-a increases, the situation un- after (or even before) eclosure of
should give a measure of security. dergoes a particular kind of appro:ach adult females.
2,8 APRIL 1967 481
 7) Males are disinclined, or unable, trol of the sex ratio normally dependent lines, an evolutionary trend to occupy
to emigrate from the batch. on the phenotype of the mother. There- such niches. The latter alternative
8) Females can store sperm; one in- fore it seems either that male-haploid seems not unlikely for the ancestors
semination serves to fertilize the whole organisms have found themselves pre- of the male-haploid groups included
egg production. adapted for life in niches of the sort in Table 1, although undoubtedly many
Arrhenotoky is a mode of reproduc- characterized by the model or that the of the cases in the Hymenoptera must
tion that readily permits the produc- evolution of male haploidy has actually be derived secondarily from relatively
tion of biased sex ratios, with con- accompanied, in several independent outbreeding species.

Table 1. Insects and mites having usual sibmating combined with arrhenotoky and spanandry. Blanks are left where clear data are not
available; in some cases equivocal evidence is mentioned in the notes.
Number
in Tendency
toward Uales e oal Thelytoky
inMF Refer-
typicaltpcl inclusion Usual
site wings
prsn pug- known in
spce(s ens
ion on site of
of pU ences
Family, genus, and species Host batch of f one present species (s),
progeny male mating nac- and
per
batch familyIOUs genus (g), (f notes

Agaontidae
Blasophaga psenes Wild fig 22 235 In fig - + (45)
Torymidae
Monodontomerus spp. Bee larva 1 12 + In host
cell. + + (46)
Pteromalidae
Nasonia vitripennis Fly pupa 2 19 Just outside
host + s (36, 47)
Encyrtidae
Dusmetia sangwani Scale insect 1 5 + In host +4 --i f (48)
Thysanidae
Thysanus elongatus Parasitoid
larvae 1 5 + ,+ g (49)
Eulophidae
Melittobia acasta Pupa of fly In host
or aculeate 1 46 + cocoon -. + + f (36, 50)
Melittobia chalybii Aculeate pupa 2 50 + In host
cocoon - + f
.+ (51)
Pleurotropis parvulus Leaf-mining Just outside
beetle larva 4 13 + leaf-mine f (52)
Trichogrammatidae
Trichogramma semblidis Alder fly
egg mass 10 60 On host + g (53)
Prestwichia aquatica Aquatic
insect egg 1 8 + In host -. s? (54)
Elasmidae
Elasmus hispidarum Leaf-mining Just outside
beetle larva 4 8 + leaf-mine (52, 55)
Mymaridae
Caraphractus cinctus Water beetle 5* 25* _
Underwater
egg it 2t near host + + f (42)
Anaphoidea calendrae Weevil egg 1 6 + + + f (56)
Anaphoidea nitens Weevil ootheca 1 3 + Just outside
host + f (57)
Scelionidae
Telenomus fariai Bug egg 1 6 + In host g (58)
Asolcus spp. Bug egg mass 8 40 + On host + + + f (37, 59)
Bethylidae
Cephalonomia quadridentata Beetle larva In group of
or pupa 1 3 + cocoons f? (60)
Sclerodermus immigrans Beetle larva 4 20 On mass of
cocoons + s? (61)
Perisierola emigrata Moth larva 2 8 In group of
cocoons f? (62)
Scolytidae
Xyleborus compactus Twig tissues 1 9 In parent
gallery + (29)
Thripidae
Limothrips denticornis Grass plant 3 20 + Grass, leaf
sheath _ f
+ (63)
Laelaptidae
Myrmonyssus phalaenodectes Moth Moth ear (64)
Pyemotidae
Pyemotes ventricosus Mother 4 86 + On mother - _--1! (52)
Siteroptes graminum Mother 7 140 + In mother - - (65)
Acarophenax tribolii Mother 1 14 + In mother- -- (35)
Tarsonemidae
Tarsonemoides spp. Mother 5 65 In scolytid's
egg niche -- (66)
* In
Dytiscus egg. in Agabtus egg.
482 VOL. 156
SCIENCE,
 No clear example of the biofacies is rather characteristic of the biofacies, group according to whether mating
has been found in the literature on the opposite combination is not so rare takes place prior to dispersion from the
arrhenotokous aleurodids and coccids. as might have been expected. Three larval host or after arrival at the new
For the coccids, an independent and species are listed in Table 1 which fit host; second, he subdivides the latter
detailed theory of the evolution of quite well in most respects but have group according to whether the males
male haploidy has already been pro- winged males and wingless females. I are usually polygynous or monogynous
posed, by S. W. Brown (20). This is see no simple explanation of this in the new borings.
based on an "island" breeding struc- anomaly, but in any case it hardly af- All three systems occur in the scolyt-
ture, with random mating within the fects the general correspondence, since, id subfamily Ipinae. The widest survey
almost-isolated subpopulations, and the from the accounts on which these list- of representatives of the first system
fact that all female coccids are wingless ings are based, it is clear that sibmating is given by Browne (28), who calls it
while males are often winged certainly usually does occur. the system of "extreme polygamy."
suggests random mating. The very com- Polygamy is extreme, but, since this
plex chromosome cycles known in vari- follows from the fact that males are
ous fungus gnats of the genus Sciara Sex Ratios with Polygyny produced in much smaller numbers
all have a common resemblance to than females, spanandry seems a better
the typical situation of male haploidy It is frequently suggested that biased term, and is used here. In all species
in that (i) virtually no chromosomes sex ratios are adaptations of the popu- of the tribes Xyleborini, Eccopterini,
of paternal origin are passed on by a lations that manifest them. In particular, and Webbini for which Browne gives
male, and (ii) the sex of an embryo the evolutionary ability to economize data, the males are not only relatively
depends on some influence transmitted in the production of males to the point few from birth but are also flightless,
by its mother (21). that gives maximum capacity for in- short-lived, and often blind. Obviously
Although all four combinations of crease (an ability which, according to this system closely corresponds to the
the winged and wingless condition ac- the model, is restricted to sibmating "extreme biofacies" discussed above;
cording to sex are known in the Sciari- lines) is sometimes imputed to any pop- some of the facts for Xyleborus com-
dae, cases in which the female alone ulation, whatever its breeding structure. pactus, the only species of these tribes
is wingless are more numerous than In one sense the idea of adaptation for which arrhenotoky has been estab-
the converse cases (22); in this respect for the benefit of the population is lished (29), are given in Table 1.
the group tends slightly toward the even less secure than that of adapta- With the other two groups consider-
condition of the coccids. Furthermore, tion for the benefit of the species. It able outbreeding is expected. Therefore,
almost entirely unisexual broods are is true that a population consisting of according to Fisher's principle, a sex
characteristic of some species, and it is numerous subgroups has many po- ratio of /2 should occur, irrespective
clear that, in these, outbreeding must tential sites for "mutation," and that of polygamy. This seems to be general-
result. It fits well with Fisher's principle "mutation" by genetic drift (for ex- ly the case. According to Browne, in
that the two types of female, arrheno- ample, the complete transience of an the Crypturgini, while Poecilips gedea-
genous and thelygenous, which exist in altruistic gene) is distinctly possible if nus clearly has the spanandrous system
these cases, are thought to be them- the subgroups are small (26). Species, (only 21 males were observed among
selves produced according to a simple on the other hand, can at least repro- 196 beetles reared in 18 broods), Car-
backcross mechanism which ensures duce in isolation from their competitors. posinus perakensis has typical "monog-
their numerical equality and, conse- The extent to which populations can amy" (28): "The young adult bores
quently fixes the sex ratio at 1/2 (23). do so without losing identity through directly out from its pupal cell"; the
Thus, the Sciaridae, like the Cocci- hybridization is not at all clear. As male is not degenerate and probably
dae, tend to support the view that the regards sex ratio, even occasional out- mates with the female in her incipient
evolution of male haploidy can take breeding should cause the breakdown new gallery, where he subsequently
place under relatively panmictic condi- of any population adaptation. Vagrant takes part in caring for the nest; and
tions. Nevertheless, with the Sciaridae, males arriving in the predominantly fe- "among 58 young adults examined, 26
the decaying plant bodies and fungi on male groups can so effectively propa- were male." It is implied (28) that
which the larvae feed are hosts of the gate the genes which caused their own the sex ratio of 1/2 holds generally with
kind specified in our model, and there production that male-producing tenden- monogamous species, and other authors
is one report (24), concerning Sciara cies must spread. This is the essence confirm this (27).
semialata, of a combination of char- of Fisher's principle. Accordingly it is With the Ipinae of the third group
acters very suggestive of the biofacies, not surprising to find that highly poly- the male flies first to the new host,
although not in its extreme form. These gynous species with outbreeding habits where he cuts a nuptial chamber. In
characters were a sex ratio of about do not have female-biased primary response to the male's attractant scent,
1/4, winglessness of males only, and the sex ratios. In polygynous mammals and several females (but not more than
Sciara habit of migrating in a compact birds a nonbreeding surplus of males eight) colonize the nuptial chamber of
column prior to pupation. Furthermore, is commonly observed during the breed- a successful male, are mated by him,
facts which similarly suggest the bio- ing season, and, in mammals at least, and construct radiating egg galleries.
facies, although somewhat less strongly, the sex ratio at birth may be actually Sex counts show a primary sex ratio
are available for gall midges of the re- male-biased. of 12 (27, 30); I know of only one
lated family Cecidomyidae (25), and With insects, evidence on this point possible exception (31). What happens
this family has unusual chromosome might be expected to come from the to the surplus males is in no case
cycles resembling those of the Sciaridae. scolytid bark beetles. Chararas (27) entirely settled. Probably their numbers
Although it is clear from Table 1 gives a classification that is useful by are somewhat reduced by the greater
that winglessness in the male sex alone biological criteria. First, he divides the hazards involved in their pioneer role,
28 APRIL 1967 483
but, at the same time, there is evidence some mating might take place before horus, except that the sex ratio is less
that many males fail to attract any dispersal, since the "polygamy" amount- extreme and males are not degenerate.
mate and die as bachelors (27, 30). ed to the observation of some mono- At leaist very occasionally the males of
With bark beetles of the hylesine gamous pairs and some lone but insemi- D. micans fly to join the female in the
nated females. But Reid found that, in new gallery (27). Evidently, as a whole
genus Dendroctonus the situation is
rather less clear. Dendroctonus frontalis, fact, less than 1 percent of the females the Scolytidae support the view that
which is monogamous, has a primary had mated before dispersal. Such a polygamy is not associated with pri-
sex ratio of ?1 (32). So does D. proportion of inbreeding certainly could mary sex ratio bias unless there is also
pseudotsugae, which is slightly poly- not explain the bias in the sex ratio, inbreeding.
gamous (33). For D. monticolae a sex but perhaps it was not typical. Another
ratio of about /3, both before eclosure species, D. micans, is quite clearly
and after attack, has been given, on on the road to inbreeding and spanan- Thelytoky
the basis of numerous counts (34). The dry. In this case the social biology
system of D. monticolae suggested that seems closely similar to that of Xyle- Browne remarked tha,t "the evolu-
tionary trend in the extremely poly-
gamous Scolytidae appears to be to-
wards the elimination of the male."
.65 He considered, however, that the oc-
currence of thelytoky in the group was
by no means proved. There is no doubt
that in the Hymenoptera similar trends
have ended in thelytoky in many differ-
ent evolutionary lines. From an evolu-
.
tionary point of view, when sibmating
is invariable, the sexual breeding system,
.60 arrhenotokous or otherwise, gives none
., (
,/ !
of the usually cited advantages over
asexual reproduction; it is in effect al-
,, ready a tree whose branches all are,
or tend quickly to become after each
t

1 mutation, completely homozygous.

. ^ ' Therefore, in a case of the extreme
~~~~~~~~~~~~,.", .."^^ biofacies, nothing of immediate impor-
.55 r~~~
ti i
I~~~~~~~~~~~~I
tance is lost by a changeover to thelyt-
oky, while convenience and perfect
.~~~~~>. economy can be gained. Table 1 shows
)
roughly the extent to which thelytoky
occurs in taxa related to the species
i] listed.
0 As noted above, the argument leading
i\
1 /a /

to (n-1)/2n as the "unbeatable" sex

.5C __"

ratio when genetic control is by fe-

X
males cannot be expected to apply ex-
w

UO
cO li
I Fig. 3. Equilibration of population sex
# ratio at /2, under conditions of random
t ;2 3 4 5 6 ' r 8 9. 10 lI 12 13 !4 ISI mating. In all cases, control of the sex
ratio is by the female, and it is assumed
; that the three genotypes GG, Gg, and gg
.4E5
6
/b'^ ~~Generation give sex ratios 1, 1/, and 0, respectively.
Dashed lines represent male haploids.
s' \1 fe^
Equilibrium frequencies of the genotypes
GG, Gg, and gg are known, by analysis,
to be as follows: in females, /2[(2)3-1],
2--(2)2, and 1/[(2)-1-1]; in diploid
, 2 8 '; D 1 2 ? 4 l males, /2, (2)3--1, and 1?2- (2). For
?, ; females, the equilibrium under male hap-
loidy is the same; for males, it is G,
1/(2)i, and g, 1-1/(2)i. Runs were
,4< _r

started by disturbing equilibrium popula-

tions as follows: males were left undis-
I/ \ turbed; for (a), all female heterozygotes
were removed; for (b), all GG and most
t t *
Gg females were removed, leaving 1 Gg
for every 999 gg. Under male haploidy
0
the approaches to equilibrium are faster
I sr and less even; but in case (a) the final
approach to the equilibrium sex ratio is
.3!5 from above-it is not oscillatory (67).
484 SCIENCE, VOL. 156
actly even to the simplest genetical Hymenoptera are in the range 14 to if to balance this, nine which were
system of inheritance. Therefore, to /2, it is thought likely that the model wholly male. In the same record there
gain some idea of how reliable the does at least exemplify the forces that were 59 groups which had just one
formula may be expected to be, the are operating. male in an otherwise female group;
case n = 2 has been investigated by statistically, this pattern, the ideal ex-
simulation on a computer. The model treme spanandry,is still very distinctive.
is deterministic, the sexual system is Occasional Outbreeding; But from this and other cases in
male-haploid, and only two alleles are Sex Ratio Games Table 1 it is evident that the typical
present. The behavior of the model occurrence of such extreme ratios does
was found to be complex, and here Among the species listed in Table 1, not necessarily imply perfect conformi-
only the results with obvious bearing Acarophenax tribolii (35) is the one ty with the biofacies in other respects.
on the unbeatable ratio are mentioned. most likely to conform, in respect of The model analysis is not applicable
When sex ratios 0.23, 0.22, and 0.21 sibmating, to the ideal biofacies. The to the sex-ratio problems arising from
were ascribed to the three female geno- males of this species usually complete the intrusion of occasional migrant
types GG, Gg, and gg, respectively, their life cycle, and die, before they males. In essential features it is ap-
from any starting frequency the popu- are born. In general the lives outlined plicable to the problem of occasional
lation went slowly homozygous for g. in Table 1 are not so secluded that double parasitismby females, and some
When the ascribed ratios were 0.22, outbreeding could not occur. For in- recently described actual cases perhaps
0.21, and 0.20, it went slowly homozy- stance, not all mating of Siteroptes provide the best evidence yet obtained
gous for G. When the ratios were graminum takes place before the rup- that, in an evolutionary sense, para-
0.225, 0.215, and 0.205, it was ap- ture of the maternal hysterosoma; gal- slitoidspecies do really play the sort of
parent that the sex ratio would equilib- leries of Xyleborus sometimes coalesce; sex-ratio game that is suggested by
rate between the two latter values. and so on. Pugnacity of males is a the model.
Thus, the unbeatable sex ratio seems to clear independent indication that out- In a number of parasitoids it has
lie between 0.215 and 0.205. Numer- breeding occurs, either through migra- been noted that more males are pro-
ous other runs of the model, with a wide tion of males or through multiple set- duced in laboratory culture than in the
variety of trios of sex ratios, gave no tling as in the model situation. The wild (39). The theory shows that, if
results contradictory to this view. males could hardly have evolved fight- crowded conditions of mass culture lead
It is not understood why the un- ing instincts if their rivals were always to an increase in outbreeding and if
beatable ratio differs from 1/4 in this of identical genotype, as brotherswould the parent sample contained sufficient
direction. There seems no reason, how- be in a long sibmated line. The ex- genetical variation in sex-ratio tenden-
ever, to think that the discrepancies treme pugnacity of Melittobia acasta cies, there could be rapid selection of
in cases n > 2 are any worse than those males (36) must indicate that it is quite the more-male-producing genes and
in the case n = 2, for it is known that common for two females to attack the shift of the general sex ratio toward
when n is infinite, corresponding to same host. With Asolcus both sexes 1/2. However this may be, several com-

panmixia, the formula correctly gives are pugnacious. The possessive fighting parative studies have shown a more
the ratio as 12. of the females when parasitizing new distinct phenomenon-that the sex ra-
It would be interesting to see how hosts (37) would tend to prevent mul- tio rises immediately when females are
some other characteristicsof the model, tiple settling-although not very effec- kept in crowded cultures. In some such
besides the unbeatable ratio, alter as tively, to judge from the behavior de- cases (see, for example, 40) experiments
n is increased. In the case of panmixia, scribed. But the pugnacity of the males indicate that this rise is due, at least
if a population sex ratio of 1/ cannot must, on the contrary, tend to cause in part, to the greater survival of male
be attained homozygously, it is yet es- outbreeding, since all but one of the larvae under conditioins of superpara-
tablished as an equilibrium, provided males released from a batch of host sitism. But recently cases have been re-
of course that the range of genotypic eggs are driven away and must at- ported in which a female, on being
sex ratios covers this value. This is tempt to acquire sexual ownership of crowded or on detecting previous para-
shown in the runs of the appropriate other batches. It is doubtless quite pos- sitism, seems to alter her oviposition
deterministic model which are graphed sible for them to do so if they find behavior so as to produce a higher
in Fig. 3. The outcome is different batches where emergence has not yet proportion of unfertilized eggs. Wylie
with the model for random settling in begun. Thus the pugnacious behavior (41) has shown that this happens in the
pairs. Thus, in a run in which the must both reflect and aggravate the case of Nasonia vitripennis. The nor-
female genotypes were assigned sex ra- biological need for it. mal sex ratio is variously given as 0.10
tios 0.4, 0.25, and 0.1, the equilibrium The somewhat anomalous cases, al- to 0.30, and this is one of the cases
sex ratio was 0.175 [p(G) = 0.25]. ready mentioned, wherein the male is where, under conditions of superpara-
With ratios 0.3, 0.2, and 0.1, there winged and the female is wingless may sitism, more male larvae survive. In
was a stable equilibrium sex ratio at be interpreted rather similarly. With spite of this usually obscurative factor,
0.267 [p(G)= 0.835]; but it wa!s evi- Dusmetia sangwani and Cephalonomia by manipulating eggs so as to prevent
dent that for some p(G) between 0.888 quadridentata,occasional outbreedingis overparasitization, Wylie showed that
and 0.999 there was also an unstable encouragednot only by the males' abili- females laid more male eggs in re-
equilibrium. ty to fly but also by the not uncommon sponse both to the detection of previ-
Although the theoretical position is occurrence of all-female groups. In C. ous parasitism and to the simultaneous
even less clear for n > 2, the ratio quadridentata, Van Emden (38) record- presence of other individuals walking
now lies, at least in some respects, with- ed, among 108 groups of progeny over the host, especially if these others
in known bounds. Since the great ma- from females known to have mated, were females. When both factors
jority of recorded sex ratios of 30 which were wholly female and, as operated together, a sex ratio of 0.59
28 APRIL 1967 485
was obtained, as against 0.20 in the in so far as it contributes to the gene
controls. More tentatively, Jackson (42) 1 1 0'9 0-6667 0-3571 0 pool at large. Evolved instincts will
reached similar conclusions with Cara- cause it to seek the highest payoff in
X\
x:
phractus cinctus. The factor of dif- the sense of expression 4; except, per-
3/4 1 1 08 0-5 01429
ferential mortality could not be con- haps, when the populationis very small,
trolled in this case, and it must be ad- it could have no interest simply in out-
mitted that, on the basis of the results 1/2 1 11667 1 0-7 0-3333 scoring its co-parasitoid. But if, on the
published, the effect in this case does contrary, the players of such a game
not seem to have been established are opponents motivated to outscore,
absolutely. The response appeared to
1'5
1/4 /1-3333 1 0'6
they would find that ?/4 is beaten by a
be connected with crowding of the higher ratio; xt, the value of x which
adults and not with perception of previ- 0 - 2-5 2 1'5 1 gives its player the greatest possible ad-
ous attack, even though an experienced vantage over the player playing x0, is
female certainly could detect such at- xo
found to be given by the relationship
x-> 0
tack, as Jackson showed. 1/4 1/2 3/4 1

In these species, double parasitism, xt = (2xo)1 - xo, (8)

Fig. 4. Sex-ratio-dependent fitness in a
at least, must certainly occur oc- pair. Numbers in the box are values of and this shows /2 to be the unbeatable
casionally in the wild. From the analy- expression 6, showing the fitness of a play.
sis given above it should be evident female using sex ratio x when her partner Relations 7 and 8 are shown graph-
uses Xo. The fitness value at 0,0 is in-
that double parasitism confronts the fe- on Fig. 4. This figure also shows
determinate;if sex ratio zero means strictly ically
male parasitoid with a difficult sex-ratio "no males produced," the value actually fitnesses (derived from expression 6)
problem. In the way in which the suc- must be between 0 and 1; but if it means as a superimposed table, and it can
cess of a chosen sex ratio depends merely "extremely few males produced," be seen that the curve of x* traces the
the value depends on the ratio x:Xo and maxima with
on choices made by the co-parasitizing
on the male's ability to fertilize a large respect to x on the im-
females, this problem resembles certain number of females-the theoretical upper plied fitness surface. If the diagram is
problems discussed in the "theory of limit of the fitness value is 3. The solid rotated clockwise through one right
games." In the foregoing analysis a and dashed lines correspond to Eqs. 7 and angle the tabulation takes the conven-
gamelike element, of a kind, was pre- 8, respectively; their significance is ex- tional forn of a payoff matrix, say W,
sent and made necessary the use of the plained in the text. showing "payoffs"to the "player"who
word unbeatable to describe the ratio has choice of row. The transpose, say
finally established. This word was ap- W0, of such a matrix would show pay-
plied in just the same sense in which can be left out of the argument. Sup- offs to the player having choice of col-
it could be applied to the "minimax" pose the parasitoid is ideally gifted and umn, and in Fig. 4 the curve of xt
strategy of a zero-sum two-person can detect not only previous parasit- traces maxima with respect to x on
game. Such a strategy should not, ism but also the sex ratio (x)) of the the surface corresponding to the ma-
without qualification, be called opti- eggs previously laid. If it lays its own trix of differences W - W0.
mum because it is not optimum against eggs to give a sex ratio x, we find, from Apart from the considerations just
-although unbeaten by-any strategy relation 4, that its fitness is propor- given, our earlier analysis (for n = 2)
differing from itself. This exactly is the tional to showed that, unless extra refinements
case with the "unbeatable" sex ratios of behavior are added, inclinations to
referred to. But whereas in the fore- - [(( -
1 +-]
xo) (1 -- x) use sex ratios aggressively as directed
X -+ Xo
going cases the "game" could be con- by Eq. 8 have no prospects under nat-
strued only rather artificially, as occur- or ural selection. Nevertheless, an arith-
ring between successive mutations act- 1 - -+ 2x (6) metical illustration of the earlier re-
x + Xo sult seems useful and leads on to an
ing rigidly in the statistical structure
of the population as a whole, we are By differentiating, the value of x interesting point. Suppose sex ratios
now concerned with a refined version which gives the highest possible value are fixed by genotype and suppose that
which is very realistically gamelike. for expression 6 is found to be given by only types giving /2 and 1/4 are present
Ability to adjust the sex ratio accord- in the population. Then the average
*- (Xo). - Xo. (7) fitness of type /4 will be some weighted
ing to clues given by the immediate
situation is undoubtedly potentially ad- Thus, the highest value x* itself can average between 1? and 1 /6. Simi-
vantageous, and it leads to individual take is 1/4, corresponding to larly the average fitness of type /2 will
females behaving as players in a literal x - /4. For xo > /4, x: < 14; be some weighted average between
sense. As an illustration, let us con- for xo < 1/4, Xo < XE < 1/4. Hence 1?3 and 1. The weights in the two
sider a hypothetical situation which is it is evident that, through trial and cases depend on the frequencies of the
simpler than the situations which para- errol, two naive players would quickly different types of pair. Thus, if pair-
sitoids like Nasonia and Caraphractus learn that constant playing of 1/4 was ing is random, the weights are the same
actually face. the optimum-yielding strategy. for both averages, being simply the fre-
Suppose parasitismcan be double but In the "game" under discussion, quencies of the types, and it is clear
no higher than double; that double however, the play of 14, although ulti- that, for all frequencies, type 14 will
parasitism brings no extra mortality; mately optimum-yielding, should be de- have the higher average (43).
and that the parasitoid must lay all its scribed as "unexploitable" rather than If pairing is nonrandom, however,
eggs in the one host. All egg batches "unbeatable." This distinction arises be- unequal weightings result. Among non-
should then be of the same size, and cause the game is not "zero-sum." random cases an interesting one is that
the actual size, if it is not too small, Biologically each parasitoid succeeds in which /2 contrives to pair off as
486 SCIENCE, VOL. 156
often as possible with 4 :1/2 then suits. But, in its failure to take into 21. M. J. D. White, Animal Cytology and Evolu-
tion (Cambridge Univ. Press, London, 1954),
spreads when 1/2 and 1/? are equally account extra mortality due to super- pp. 239-246.
22. F. W. Edwards, Entomologist's Monthly Mag.
common, although it is still unable to parasitism, the fact that females lay 70, 140 (1934).
do so when it is very rare or very com- varying numbers of eggs and may move 23. C. W. Metz, Am. Naturalist 72, 485 (1938).
24. F. W. Edwards, Entomologist's Monthly Mag.
mon. But if a genetic type could dis- on from one host to another, and so 49, 209 (1913).
sort in this way it should easily evolve on, the basis is certainly much too 25. H. F. Barnes, Gall Midges of Economic Im-
portance, vols. 1-6 (Crosby Lockwood, Lon-
the further ability to adjust its sex ra- simple. Obviously the formulas do not don, 1946-56).
tio according to whether it was paired check with Wylie's results, since they 26. S. Wright, Ecology 26, 415 (1945).
27. C. Chararas, -tude biologique des Scolytides
with its own type or with the other cannot account for sex ratios above 14?. des Coniferes, Encyclopedie Entomologique
(Lechevalier, Paris, 1962).
type, and then if it played 0 in the In fact the ratio of 0.59 Wylie ob- 28. F. G. Browne, Malayan Forest Rec. 22, 1
former case and ?/ [or, even better, tained in one experiment is too high (1961).
29. P. F. Entwistle, Proc. Roy Entomol. Soc.
(2xo) I-x] in the latter, it would even to be the best ratio for the out- London Ser. A 39, 83 (1964); 14 percent of
spread easily at all frequencies of oc- scoring game. But the variability of broods had no male.
30. M. W. Blackmain, N.Y. State Col. Forestry
currence against any nondiscriminating Wylie's ratios from ratios for controls Tech. Pub. 16, No. 1, 11 (1915); D. L. Wood,
and the fact that his experimental stock Pan-Pacific Entomologist 38, 141 (1962).
type. Comparable evidence for polygynous birds
No such refined discrimination can was not fresh from the wild (where is cited by J. Verner and M. F. Willson
[Ecology 47, 143 (1966)].
be expected in parasitoids. Ability to triple parasitismshould be very uncom- 31. G. R. Hopping [in Can. Entomologist 94, 506
detect whether a host is already parasi- mon) also discourage hope of any de- (1962)] reports the existence of a thelygenous
strain in Ips tridens. Such strains are unlikely
tized is well known, but no clear case tailed check. It can only be said that, to be widespread in the genus (compare the
where a female is able to assess even in its direction, the effect that Wylie "sex ratio" traits of Drosophila pseudoobscura
and its allies).
the quantity of previous parasitism has and Jackson have independently re- 32. E. A. Osgood, Jr., and E. W. Clark, Can. En-
tonmologist 95, 1106 (1963).
yet been reported (44); therefore, ability ported accordswith the theory. 33. J. P. Vit6 and J. A. Rudinsky, Forest Sci. 3,
to assess sex ratio is extremely im- 156 (1957).
References and Notes 34. R. W. Reid, Can. Entomologist 90, 505 (1958).
probable. However, although this limits 1. R. A. Fisher, The Genetical Theory of Na-
35. R. Newstead and H. M. Duvall, Roy. Soc.
the precision with which a parasitoid tural Selection (Dover, New York, ed. 2, Rep. No. 2 of Grai,n Pests (War) Committee,
London (1918). A report by E. A. Elbadry
can take advantage of a predecessor 2. W. 1958), p. 158. and M. F. S. Tawfik [in Ann. Entomnol. Soc.
F. Bodmer and A. W. F. Edwards, Ann.
use of it does A,n. 59, 458 (1966)] shows that Adactylidium
(in theory, by Eq. 7), Human Genet. 24, 239 (1960); W. A. Kolman,
has biology very similar to Acarophenax.
Amn. Naturalist 94, 373 (1960).
not lessen the gamelike character of 3. J. Verner, Am. Naturalist 99, 419 (1965). 36. G. S. Graham-Smith, Parasitol. 11, 347 (1919).
37. F. Wilson, Australian J. Zool. 9, 737 (1961).
the situation, or even change the un- Verner claims to show that, given factors
38. F. Van Emden, Z. Morphol. Oekol. Tiere 23,
causing fluctuations of the population's pri-
beatable ratio for the case of groups mary sex ratio, a 1:1 sex-ratio production
425 (1931). Even in the absence of occasional
proves the best overall genotypic strategy. outbreeding, all female batches are not neces-
always of a fixed size. 4. W. D. Hamilton, J. Theoret. Biol. 7, 17 sarily doomed. Unmated females of Cepha-
With the case of occasional double (1964). lonomia quadridentata produce daughters after
5. E. Novitski, Genetics 32, 526 (1947). mating with their sons. This ability is wide-
parasitism likewise it may be seen that 6. L. C. Dunn, Science 144, 260 (1964); L. spread among arrhenotokous organisms, and
game-theory considerations apply and Sandler and Y. Hiraizumi, Can. J. Genet. is developed into a remarkable adaption in
Cytol. 3, 34 (1961). Melittobia acasta [see F. B. Browne, Parisitol.
prescribe definite policies. Evolved tend- 7. W. A. Hickey and G. B. Craig, Jr., Genetics 14, 349 (1922)]. Xylebor,ts compact-us has the
encies will be such that first-comers 53, 1177 (1966); Can. J. Genet. Cytol. 8, 260 ability, and data suggest that it must be fre-
(1966). quently used in nature [see note 29]. In
to the host will use a sex ratio less 8. D. F. Owen, Heredity 21, 443 (1966). Podapolip,ts dia,nder the female is regularly
9. B. Wallace [in Evolution 2, 189 (1948)] docu- mated by a precocious son arising from
female-biased than the workable ex- ments an actual case of X-linked sex-ratio her first egg [M. Volkonsky, Arch. Inst.
treme in order to allow for the chance drive. J. B. S. Haldane and S. D. Jayaker [in Pasteur Algerie 18, 321 (1940)].
J. Genet. 59, 29 (1964)] give conditions for 39. C. P. Clausen, J. N.Y. E,nto,m,ol. Soc. 47, 1
that double parasitism will occur. The equilibrium: a driving sex chromosome X' is (1939).
first-comers'best sex ratio will depend not arrested unless XX' is more fit than 40. G. Salt, J. Exp. Biol. 13, 363 (1936). This
X'X' by at least 1/3. effect accords with Fisher's principle. Super-
both on this chance (p, say), and on 10. H. D. Stalker, Genetics 46, 177 (1961). parasitism brings unlike genotypes together
the sex ratio that second-comers can 11. S. W. Brown, Scie,nce 151, 417 (1966). and causes at least partial outbreeding; there-
12. G. D. Hanks, Genetics 50, 123 (1964). fore, since males are scarcer, they are under
be expected to use. The second-comers' 13. J. D. McCloskey, Anm. Naturalist 100, 211 more intense selection for competition ability.
(1966). 41. H. G. Wylie, Canm. Enrtomzologist 98, 645
best sex ratio, assuming they can detect 14. A. S. Parkes, in The Numbers of Man and (1966).
previous parasitism, will be based only of Animals, J. B. Cragg and N. W. Pirie, 42. D. J. Jackson, Trans. Roy. Ento,m,ol. Soc.
Eds. (Oliver and Boyd, Edinburgh, 1955); G. London 118, 23 (1966).
on the expected sex ratio of the first- Sundell, J. Emb. Exp. Morphol. 10, 58 (1962); 43. A similar argument shows that the play 0
comers. Hence it can be shown either The work of J. A Weir [Genetics 45, 1539 also loses to the play /4. The combination
(1960)] emphasizes the importance of the 0,0 gives the highest possible payoff to the
by game-theory reasoning (each indi- father in determining sex ratios in the group (namely, 4), so this "solution" should
vidual supposedly considering the intel- mouse. be favored by a "group-selectionist." From
15. E. Schilling, J. Reprod. Fertility 11, 469 what has been said, the "solution" ?/2,?, with
ligent policy of the other) or, more (1966). group payoff 2, should be favored by the
16. D. Lewis, Biol. Rev. Catmbridge Phil. Soc. extreme believer in biological bellum omnittm
realistically,by supposed behavior grad- 17, 46 (1942). contra omnnes. It is pleasing, therefore, to find
ually "learned" by the species through 17. A. Wilkes, Science 144, 305 (1964); Can. that what turns out to be the true solution
Entomologist 97, 647 (1965). in this case, 1/4,1/4. lies exactly midway be-
natural selection, that, in the idealized 18. If each haploid male can mate with k females tween the others, both in position and in
conditions we are considering, the fol- and if mated females produce sex ratio e, payoff.
some females fail to be mated if k < (1-e)/e. 44. G. Salt, Symnp. Soc. Exp. Biol. 15, 96 (1961).
lowing responses will finally become es- Such cases finally have a regular alternation 45. G. Grandi, Boll. Lab. Entomol. Roy. Inst.
tablished: first-comerswill use sex-ratio of sex ratios between e and 1-ke. Between Suiper. Agr. Bologna 2, 1 (1929).
these values there is an unstable sex ratio 46. P. Rau, Ann. Enitonmol. Soc. Amer. 40, 221
p2/(l + p)2 and second-comers will equilibrium at /2 (2 + kf - [kf(4 + kf)]1}, (1947); J. H. Fabre, Souvenirs Entomologi-
use p/(1 + p)2. Thus, a first-comer, where f 1 - e. In 1917 C. B. Williams ques 3, 179 (1886).
gave arithmetical models showing alternation 47. A. A. Moursi [Bull. Soc. Fouad Inst. Entomol.
because of the handicap of its uncer- [J. Geniet. 6, 189 (1917)] and A. F. Shull 30, 21 (1946); ibid., p. 39] reported very rare
published observations suggesting that alter- thelytoky.
tainty, has lower fitness than a second- nations may occur in thrips in the wild 48. M. F. Schuster, Ann. Entomol. Soc. Aner.
comer. [Genetics 2, 480 (1917)]. 58, 272 (1965).
19. W. F. Bodmer and A. W. F. Edwards, Ann. 49. C. P. Clausen, Univ. Calif. (Berkeley) Pub.
It might be hoped that these two Human Genet. 24, 239 (1960). They imply (I Entomol. 3, 253 (1924).
formulas would give a basis for check- think incorrectly) that there is a possible 50. F. B. Browne, Parisitol. 14, 349 (1922). These
situation for which their analysis is exact. are feeble, reluctant fliers.
ing the theory against experimental re- 20. S. W. Brown, Genetics 49, 797 (1964). 51. E. R. Buckell, Pan-Pacific Entomologist 5, 14
28 APRIL 1967 487
 (1928); R. G. Scmieder, Biol. Bull. 74, 256 57. M. C. Mossop, Unioi S. Africa Dept. Agr. 64. A. E. Treat, Proc. 10th Intern. Congr. En-
(1938). The sex ratio is of Scmieder's second Sci. Bull. No. 81 (1929). tomology 2, 475 (1956).
form. 58. A. de Costa Lima, Inst. Oswaldo Cruz Meme. 65. K. W. Cooper, Proc. Nat. Acad. Sci. U.S.
52. T. H. C. Taylor, The Biological Control of 21, 201 (1928); A. Dreyfus and M. E. Breuer, 23, 41 (1937).
an Insect in Fiji. An Account of the Coconut Genetics 29, 75 (1944). Sex ratio for Triatoma 66. E. E. Lindquist and W. D. Bedard, Can.
Leaf-mining Beetle and Its Parasite Complex megista hosts. Entomologist 93, 982 (1961).
(Imperial Institute of Entomology, London, 59. Sex ratio for Asolcus basalis. A definite tend- 67. The results of Bodmer and Edwards [in Ann.
1937). ency toward the inclusion of at least one Human Genet. 24, 239 (1960)] on rate of
53. G. Salt, Parasitol. 29, 539 (1937); ibid. 30, male among eggs laid in a host by A. approach to equilibrium do not apply in
511 (1938). The males are winged when bred semistriatus has been observed by M. Javahery detail to such extreme genetical cases as
on hosts other than Sialis. (personal communication). those of Fig. 3. In general it is true, as these
54. F. Enoch, Entomologist's Monthly Mag. 34, 60. F. Van Emden, Z. Morphol. Oekol. Tiere 23, workers concluded, that rate of approach
152 (1898). M. Rimsky-Korsakov [Rusk. En- 425 (1931). The males are dimorphic; some depends positively on the variance [in the cases
tomol. Obozr. 16, 211 (1917)] reports that are apterous. shown, AX/(2 - X) is ultimately 2.086V for
females are dimorphic; some are apterous. normal reproduction and 2.88V for male
61. J. C. Bridwell, Proc. Hawaii Entomol. Soc. 4,
K. L. Henriksen [Ann. Biol. Lacustre 11, 19
291 (1920). Aptery occurs, but rarely. C. E. haploidy]. But if, for example, Gg gives all
(1922)] suggests the existence of a thelytokous Keeler [Psyche 36, 41 (1929); ibid., p. 121] females, as in Sciara coprophila and Chryso-
race; like R. Heymons [Deut. Entomol. Z. found a thelytokous race. myia rufifacies [C. W. Metz, Am. Naturalist
1908, 137 (1908)], he observed fewer males, 72, 485 (1938); F. H. Ullerich, Chromosoma
and no mating in the host egg. 62. H. F. Willard, U.S. Dept. Agr. Tech. Bull. 14, 45 (1963)], equilibrium is reached im-
55. The sex ratio (from cols. 3 and 4) is typical 19, 1 (1927); A. Busck, Insecutor Inscitiae mediately.
for 3rd-instar hosts. menstruus 5, 3 (1917). 68. I thank Dr. D. Bevan for information about
56. A. F. Satterthwait, J. N.Y. Entomol. Soc. 39, 63. E. Pussard-Radulesco, Ann. Ephiphyties 16, bark beetles and Dr. T. Lewis for information
171 (1931). 103 (1930). about thrips.

NEWS AND COMMENT generally come under the heading of

"science and society." And, as an in-
stitution, it still tends to be tone-deaf
to these concerns. Recently, for ex-
ample, 127 Academy members joined
The National Academy of Sciences: several thousand scientists in petitioning
President Johnson to order a study of
Profile of an Institution (III) chemical and biological weapons
(CBW). There is no legal or technical
impediment to the Academy's studying
at least the nonclassified aspects of this
Two principal positions exist on the ably aspire to take up complex issues subject on its own initiative. But, in
use that the National Academy of Sci- and arrive at positions that reflect the raising the CBW issue the petitioners
ences should make of what are consid- informed conclusions of the member- obviously hoped to encourage the ad-
ered to be its greatest assets, prestige ship. They also point out that the ministration to renounce the use of such
and public confidence. Academy possesses a modest mandate weapons. Johnson was not inclined to
The first position is centered on the -to advise when advice is requested. snap at the bait, and the Academy was
belief that the Academy should active- No one need request the Academy's not inclined to volunteer itself into the
ly, and, if need be, on its own initiative, advice, nor, having requested it, need middle of a controversy over CBW.
use these assets to promote the progress one follow it. Furthermore, they note When it comes to issues that can offend
and wise use of science and technology. the Academy has very limited resources those capable of counterattack, the
In a period of limited expansion of fed- for addressing itself to matters outside Academy still tends to avoid looking
eral support for scientific research, some the interest of its clients. Its income for trouble. Furthermore, as an ad-
advocates of activism would like to see from endowment last year came to visory organization it prefers (and so
the Academy devise and recommend $398,000-as compared with $19.4 its clients have come to realize) chew-
priorities for allocating the available million that it received in grants and able problems-clear-cut issues con-
funds. Concerning the uses to which contracts from its advice seekers. (The cerned with how something might be
science and technology are put, there Academy pays its way mostly with done, or what will be the consequences
are persons in this camp who would overhead fees, usually 28 percent, that of doing it, not with whether something
like to see the Academy initiate studies it charges its customers.) Therefore, the should be done.
and issue pronouncements on contro- holders of this viewpoint believe, the Nevertheless, a careful examination
versial matters such as missile defense Academy should not go out hunting for leads to the conclusion that here and
and chemical and biological weapons. trouble; rather, it should husband its there things are stirring inside the ven-
The second point of view is repre- prestige and reputation so that it will erable institution, and at a few points
sented by those who contend that, how- command respect when it deals with there is even to be found a definite
ever desirable such a role may be, the issues that come its way. spirit of adventure. While the signifi-
Academy can never be an effective ve- Now, until quite recently the second cance and potential of these develop-
hicle for carrying it out. They argue camp wholly prevailed in Academy af- ments are difficult to assess, it is clear
that prestige and confidence are fragile fairs. As an institution, the Academy that the affairs of the Academy are no
commodities that are rarely enhanced has always been tone-deaf to the con- longer wholly dominated by cautious
by frequent involvement in controversy. cerns that produced offshoots of the traditionalists, for in five separate and
They emphasize that the Academy is scientific community such as the Fed- most important areas there have been
not a representative body; that, with its eration of American Scientists and other changes and activity that in many re-
diffuse membership, it cannot reason- organizations concerned with issues that spects point the way to a significant
488 SCIENCE, VOL. 156