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THE 

AMERICAN NATURALIST 

Vol. XLVIII October, 19 U No. 574 

SEX -LIMITED AND SEX-LINKED INHERITANCE 

PROFESSOR T. H. MORGAN 
Columbia University 

Darwin used the expression ' ' inheritance as limited by 
sex" to include all cases in which a character is peculiar 
to one sex. His list of such cases 'covers in the main the 
group of secondary sexual characters. Darwin's expres- 
sion has been contracted to sex-limited inheritance, and is 
widely employed to-day in the same general sense in which 
Darwin used the expression. For instance, Bateson in 
his book "Mendel's Principles of Heredity" includes 
both horns in sheep and color blindness in man as sex- 
limited characters. 1 

Now that the inheritance of several of these cases has 
been definitely worked out, it has become increasingly evi- 
dent that such characters as color blindness, and haemophi- 
lia in man, the twenty-five " sex-linked " characters in Dro- 
sophila, and certain characters in birds and in butterflies 
follow a law of inheritance that is essentially different 
from that followed by some of the other cases. It has 
become necessary, therefore, to recognize two groups of 
cases that differ fundamentally in regard to their heredity. 
To one of these groups I have applied the term sex-linked 
inheritance, and, for the present at least, we may still make 
use of the older expression sex-limited inheritance (and 

1 See pp. 169-174 in section headed "Heredity Limited by Sex; the Horns 
of Sheep," where the term sex inheritance limited descent (p. 172) also 
appears. 

577 



578 THE AMERICAN NATURALIST [Vol. XL VIII 

sex-limited character) to cover that class of cases (obvi- 
ously a. very mixed one which will be broken up as our 
knowledge regarding it becomes more certain) that in- 
cludes largely, as originally intended, the secondary sexual 
characters. 2 In those cases of sex-linked inheritance, in 
which the male is heterozygous for the sex factor, the 
grandfather transmits his peculiarity, through his daugh- 
ters, to half of his grandsons only; and reciprocally an 
affected female transmits her peculiarity to all her sons, 
and, through her sons bred to her daughters, to half of 
her granddaughters and to half of her grandsons 3 . More- 
over the appearance of the character in the female is not 
exceptional or abnormal, as is sometimes implied in cases 
like color blindness in man, for, the character can always 
be transferred from the male to the female by suitable 
crosses. 

On the other hand, there are cases in which a character 
appears in one sex only— the character is limited, there- 
fore, to the male or to the female. Such cases may be 
properly called sex-limited, and were so called by Darwin. 
As typical examples I may cite the horns of certain races 
of sheep that are present in the ram and absent in the 

2 Gt. H. Shull has recently said (Zeii. Ind. Ahst. xmd Vererb., XII, 1914, 
p. .160) that, in his opinion, it would be better to retain the term sex-limited 
for those cases that I call sex-linked and call other cases secondary sexual 
characters. This view is not historically in accord with Darwin's usage of 
the term "limited by sex." This fact, in itself would be a sufficient argu- 
ment for rejecting Shull 's suggestion, but, in addition, the term sex limited 
is an actual misnomer for the class of cases to which he proposes to apply it. 
There are eases like the eosin eye of DrosopMla that differ in the male and 
female in the same way as do many secondary sexual characters (in fact they 
are such in a descriptive sense) but nevertheless show sex-linked inheri- 
tance. Since a new name is required to express our fuller information in 
regard to some of the characters that were originally included under the 
older term, why not begin by adopting suitable and expressive ones. 

s In those cases in which the female is heterozygous for a sex factor, as 
in birds and in butterflies, the same principle is involved but the sequence is, 
in a sense, reversed; thus the grandmother transmits, through her sons, her 
peculiarity to half of her granddaughters; and reciprocally, the affected 
male transmits his peculiarity to all of his daughters, and, through his 
daughters bred to his sons, to half of his grandsons and to half of his grand- 
daughters. 



No. 574] INHERITANCE 579 

ewe (or else more developed in the ram than in the ewe) ; 
the color of butterflies like Pafiilio Memmon, with three 
types of females ; and the dark spot on the abdomen of the 
male of the bug Euchistus variolarius. These characters 
can not be transferred through the gametes to the female 
of their own race by any known combination. 

Whether one likes or does not like the particular terms 
used to denote these two classes of cases, the fact remains 
that there are two such categories, and to ignore their 
existence is only to make obscure a distinction that is per- 
fectly plain. 

Concerning the mechanism involved there is something 
more that may be said. It has been sufficiently shown in 
the case of sex-linked inheritance that the sex-linked char- 
acter follows the known distribution of the sex chromo- 
somes. It is unnecessary to repeat here the abundant 
evidence in support of this statement. The simplest inter- 
pretation of this known relation is that the character is 
dependent for its realization on the sex chromosomes. I 
do not mean, of course, that the sex chromosomes alone 
produce the character but that something in these chromo- 
somes, some "factor," acting in conjunction with the rest 
of the cell, conditions the character. 

On the other hand, in the case of sex-limited characters 
the facts can not be explained on the assumption that the 
characters follow the sex chromosomes. It is clear that 
they do not do so. But we can give a consistent interpre- 
tation of the facts if we assume that sex-limited characters 
follow the distribution of the ordinary chromosomes. 

Since this relation has recently been not understood 
and misinterpreted I may be pardoned, I hope, for taking 
up the question once more. 

"Wood crossed horned Dorset sheep with hornless Suf- 
folks. The sons had horns, the daughters lacked them. 
Inbred these gave in the F 2 generation— horned <$, 3; 
hornless <$, 1; horned % 1; hornless 2, 3. Bateson and 
Punnett have shown that the results are explicable on the 
basis that one factor for horns in the male produces 



580 THE AMERICAN NATURALIST [Vol. XL VIII 

horns but one factor is insufficient in the females. This 
conclusion was put to the test by breeding an F x hornless 
ewe to a hornless ram. The F 1 ewe should be hetero- 
zygous for the factor for horns, and, therefore, when she 
is bred to a homozygous hornless ram, half of her off- 
spring should be heterozygous for hornlessness and half 
homozygous for hornlessness. Since half of her sons 
should have a factor for horns they are expected to 
develop horns, and this is what occurred. Half of the 
daughters also should have a factor for horns, but should 
not develop horns, and this also was true. 

It has been recognized for several years that this and 
related cases can not be explained on the assumption that 
the factors- involved are carried by the X or by the Y 
chromosomes. But we can interpret the statement that 
one factor for horns is sufficient in the males to call forth 
horns, but not sufficient in the female "in terms of chromo- 
somes," if a factor for horns is carried by one of the 
■chromosomes other than the sex chromosome. In other 
words we need only appeal to a mechanism with which we 
are familiar to cover the results. 

The second illustration is furnished by the recent 
experiments of Foot and Strobell, and since the authors 
have rejected the chromosome hypothesis as inapplicable 
to their results, and since in the case of insects the condi- 
tions are simplified because castration experiments have 
shown that the sex glands are not themselves responsible 
for the secondary sexual characters, we may profitably 
consider this case even more fully. 

In one of the bugs, Euchistus variolarius, the male has 
a black spot on the abdomen. The female lacks the spot. 
A female of this species was crossed to a male of another 
species, viz., Euchistus servus, having no spot in either 
sex. The daughters had no spot, the sons had a spot 
fainter than that of variolarius. Inbred these gave, in F 2 , 
249 females without a spot, 107 males with a spot (devel- 
oped to different degrees) and 84 males without a spot. 
The F x results show that one factor for spot in the male 



No. 574] INHERITANCE 581 

suffices to call forth in some degree the spot in the hybrid. 
Its intensity varies from a condition approaching that in 
pure variolarius to a faint spot (possibly even to no spot 
at all). The F x results show also that a single factor in 
the female fails to cause the spot to develop in that sex. 
In the Fj male the failure of the spot to reach in most 
cases its full development shows obviously that the same 
conditions that produce a male that is perfect so far as 
his sex gonad is concerned, do not suffice to cause the full 
development of the spot, although the factor for the spot 
is present in one dose at least. The only confusion that 
is liable to arise is that in none of the F 2 females did the 
spot appear, although in some of them there must have 
been a double dose of spot. But the difficulty is imaginary 
as a little thought will show. In the first place the female 
of E. variolarius herself does not show the spot, yet this 
female must have a double dose of spot if spot is in the 
X chromosome or in any other chromosome (except the Y). 
Foot and Strobell by an elaborate analysis of the case 
show that the factor can not be carried by either the X or 
the T chromosome. It is unnecessary to repeat their 
argument ; for, if the factor were carried by the X chromo- 
some, only half of the grandsons should show it, while, in 
fact, many more than half of them show it; and it could 
not be earned by the Y chromosome because the Y chromo- 
some of variolarius is not present in the female, hence 
could not have entered the cross as made. We are con- 
cerned then only with a third possibility, viz., that there is 
something in the female condition itself that is inimical to 
the development of the spot. Since neither X nor Y 
carries the factor in question it must be present in duplex 
in the female of variolarius (if every gamete must have it 
in simplex and the experiment shows that this is the case), 
and since the spot does not shoiv in the female of vario- 
larius, it is obvious that it can not appear in that sex even 
in duplex. If it be granted that the character is like other 
Mendelian characters, and the authors' evidence shoiv that 
it is inherited as are Mendelian characters, the conclusion 



582 THE AMERICAN NATURALIST [Vol. XLVIII 

is self evident; for,, in demonstrating that all of the 
gametes of variolarius carry spot the authors actually 
destroy their oivn argument. 

It only remains to point out some of the different ways 
in which a factor being present in duplex both in the male 
and in the female produces its effect only in the male. In 
some cases it has been shown that the ovary produces 
some substance that is inimical to the production of cer- 
tain characters. For instance in fowls and in ducks the 
presence of the ovary suppresses the development of 
the male plumage. That the factors for the male plumage 
are present is shown by its development when the ovary 
is removed. But in some insects it has been found that 
neither the ovary nor the testis produces these kinds of 
substances; for, when the testis or the ovary is removed 
the secondary sexual characters are not affected. Here 
the mode of explanation must be different. But the con- 
ditions, or complex, or factors that produce the ovary in 
the female are acting in every cell of the body, and con- 
sequently an effect, that is indirectly caused in the fowl 
or duck, might be directly caused in the insect. For, each 
cell is a chemical factory. Such a factory may help to 
produce an ovary and the ovary produce a substance that 
demonstrably suppresses the male plumage, or the same 
kind of factory may do similar work through the activity 
of some other part of the body, or conceivably it may do 
its work in every cell of the body. This it seems to me is 
the most reasonable view to take of the matter in the case 
of the variolarius-servus cross. We can express the same 
thought in symbols by representing the female of vario- 
larius by XXAABBCODDSS, etc., and the male by 
XYAABBCCDDSS, etc. The chemical interaction be- 
tween two X's and the rest of the cell is of such kind that 
it produces a female, and the female complex, as such, is 
inimical to the development of a spot and favorable for 
the development of the accessory organs of reproduction 
and of all secondary sexual characters of the female, while 
XY and the rest of the cell is inimical to the development 



No. 574] INHERITANCE 583 

of the acessory organs and of the secondary sexual char- 
acters of the female, and favorable for the development of 
the accessory sexual organs and of the secondary sexual 
organs of the male. This view is of course compatible 
with the idea that there may be special factors for these 
organs in chromosomes other than the sex chromosomes, 
and the view holds both in a general way and on the 
special chromosome hypothesis as well. 

To assume that all the factors for characters that are 
shown by the male or by the female must be carried by a 
sex chromosome of some kind, if carried at all by chromo- 
somes, is a travesty of the point of view of those who hold 
to the chromosome hypothesis as a reasonable working 
hypothesis to account for Mendelian inheritance. Just 
as it has been shown that there are factors in the sex 
chromosomes that affect many parts of the body, that are 
not concerned with differences of sex; so, on the other 
hand, the evidence shows that there are factors in other 
chromosomes that are influential in producing secondary 
sexual characters.