Evolution__3rd_Edition

398 PART 4 / Evolution and Diversity
Box 14.1
Haldane’s Rule is Probably (at Least in Part) Explained by the
Dobzhansky–Muller Theory
Postzygotic isolation in the Dobzhansky–Muller theory is caused by
interactions between genes at many loci. Let us see what happens if
one of the loci is on the X chromosome and one on an autosome
(Figure B14.1). The two parental species have internally satisfactory
combinations of genes, but the hybrid offspring contain gene
Parental
species
Hybrid
species
Species 1
X1 A1 A1
Y1/ X1 A1 A1
X1 A1 A1
X2
A2 A2
Species 2
X2 A2 A2
Y2/ X2 A2 A2
X1 A1 A1
Y 2 A2 A2
Female Male
Figure B14.1
The “dominance theory” of Haldane’s rule. Some gene
combinations in hybrids will be new and incompatible:
for example, X 1 /A 2 combinations (where X 1 /A 2 refers to
a combination of one gene on the X chromosome from
species 1 and another gene on an autosome of species 2).
If the incompatible gene on the X chromosome is recessive
then the gene combination will not be expressed in female
hybrids (the X 2 gene is dominant) and female hybrids are
alright. But in male hybrids the X 1 /A 2 combination is
expressed because the male lacks an X 2 chromosome.
Males have reduced fitness. The theory is illustrated as if
for a fruitfly, in which males are heterogametic. In a species
in which females are heterogametic, “males” and “females”
would need to be reversed.
combinations that are incompatible. A gene on the X chromosome
of species 1 (X 1 ) may be incompatible with a gene on an autosome
of species 2 (A 2 ). What matters is whether the defect caused by the
incompatibility between X 1 and A 2 is dominant or recessive. If it is
dominant, it will damage both male and female hybrid offspring; if it
is recessive it will damage male but not female offspring. Thus the
standard Dobzhansky–Muller theory can explain Haldane’s rule
with the added assumption that some of the genes at work on the X
chromosome are recessive. In all, we explain Haldane’s rule by two
genetic properties: (i) postzygotic isolation is due to interactions
between many gene loci (that is, epistasis), and some of these gene
loci will be on the X chromosome; and (ii) some of these X-linked
genes are recessive.
This is called the “dominance” theory of Haldane’s rule. It works
well for genes causing inviability in fruitflies. However, it is probably
not a complete explanation. The genetic explanation for cases in
which the heterogametic sex of hybrid offspring are inviable
probably differs from cases in which they are sterile. Genes that
influence viability usually affect males and females equally, because
they are genes that influence the well-being of the whole body.
Male bodies do differ in some respects from female bodies, and
some genes do influence viability in only one gender; but these
genes are exceptional. The genes that influence fertility, by contrast,
mainly differ in male and female bodies. Genes influencing female
fertility are expressed in the ovaries and influence oogenesis; these
genes are switched off in male bodies. Some explanation other than
the simple dominance theory given here may be needed for cases of
sterility that fit Haldane’s rule. Also, the theory as given here works
for the kind of X chromosome dosage compensation that is found in
fruitflies, but the theory needs to be extended to explain mammals.
Therefore, the Dobzhansky–Muller theory can be used to explain,
at least in part, the longstanding and well documented
generalization known as Haldane’s rule. Haldane’s rule has been a
topic of active research recently, particularly since a classic
experiment by Coyne (1985). Haldane’s rule has proved to be an
excellent route to understanding the genetic changes that cause
speciation, or at least that cause postzygotic isolation.
Figure 14.8b, not Figure 14.8a. Postzygotic isolation evolves faster in the heterogametic
gender. But what is the explanation for Haldane’s rule? The question has been the topic
of active research recently, and many detailed genetic hypotheses have been tested.
Box 14.1 describes how the basic Dobzhansky–Muller theory can explain Haldane’s
..