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AMONG Australia’s famous marsupials live many unsung native rodents.
Arguably the most bizarre are the hopping mice, members of the genus Notomys.
Dwelling largely in the arid zone, these animals have big eyes and ears,
a long brush-tipped tail and extremely long hind limbs and feet that enable
them to hop rapidly across the open sand. But what makes the hopping mice
especially peculiar – and peculiarly interesting – is their strange reproductive
anatomy.

A sexually mature male hopping mouse has remarkably small testes. The
biologists who first found and described these animals never commented on
this fact, but perhaps they thought that all the males they collected were
reproductively inactive, even though they collected some pregnant females
as well. Our research has concentrated on a captive colony of spinifex hopping
mice at the University of Adelaide. Usually, rodents in the murid group,
which includes laboratory rats or mice and even most native Australian species,
have large and conspicuous testes carried in scrotal sacs. But in these
hopping mice, the testes can be a twentieth the size of those in most other
species of similar body size.

Most rodents also have large ‘accessory’ sex glands. Often the most
noteworthy are the seminal vesicles, whose secretions form the large copulatory
‘plug’ which the males deposit in the vagina after ejaculation to facilitate
the passage of sperm into the uterus. In the spinifex hopping mice, the
situation is quite different. They have only one large accessory sex gland,
the bilobed ventral prostate: all the other glands, including the seminal
vesicles and coagulating glands, are minute. Not surprisingly, the males
do not deposit a large, hard copulatory plug in the vagina during mating.

In addition to these obviously unusual features of the reproductive
anatomy, more subtle peculiarities are evident under the microscope. In
most rodents (and most mammals too), spermatozoa from the testes mature
as they pass down a long, tightly coiled tube known as the epididymis. Sperm
finally come to reside in its tail, the cauda epididymis, where vast numbers
remain until ejaculation. In the hopping mice, by contrast, the epididymis
is remarkably short, is not as highly coiled, and no dense mass of sperm
accumulates in the cauda. The tube that connects the cauda to the urethra
that leads to the outer world, the vas deferens, is also unusual: its lower
half lacks the usual thick muscular coat and its lining is greatly infolded.
Sperm are stored around the middle of its length. The sperm produced by
any one animal are far more variable in structure than in most other rodents,
even more so than in strains of laboratory mice that have been used to investigate
the causes of variation in the structure of sperm.

A hopping mouse’s penis is also highly unusual. Most rodents have a
barrel-shaped penis with small, backward-pointing spines. When erect, it
forms a deep cut at its end that may help the male to place the copulatory
plug against the female’s cervix. In the spinifex hopping mouse, the penis
has a very thin shaft, but the spines are up to three times as long as those
in most other rodents. In addition, it does not form a cup at its tip when
erect.

So every anatomical feature of the male reproductive apparatus of the
hopping mouse is unique in its structure and unlike that of its relatives.
But how could such structures have evolved? One of the first questions was
whether the anatomy of the lower region of the female tract is coadapted
to that of the male. And, associated with this, does any aspect of their
copulation relate to this anatomy? The answers we found were dramatic. In
all rodents in the genus Pseudomys and in the common laboratory rodents,
the vagina invariably had a large lumen surrounded by several longitudinal
folds backed by a very thin coat of muscle. In hopping mice, the lumen of
the vagina is much smaller, usually oval-shaped in cross section, and its
lining lacked folds for much of its length and was surrounded by a thick
coat of muscle. The cervix, rather than being a bulky, fibrous structure,
was barely distinguishable from the vagina.

At about the time of these investigations, we sent some animals to Don
Dewsbury of the department of psychology of Florida State University. He
had speculated from studies of muroids in the New World that species that
have reduced accessory sex glands are more likely to ‘lock’ during copulation.
To test these predictions in a separate group of rodents, Dewsbury wanted
to investigate hopping mice. As predicted, he found that locking does indeed
take place during mating, and lasts for up to two-and-a-half minutes – the
first murid rodent observed to copulate in this way. So it seems likely
that the large spines on the penis, together with the narrow lumen of the
vagina and its thick muscular coat, are adaptations for locking. Further,
the absence of the large seminal vesicles and coagulating glands in the
males, which preclude the formation of a large copulatory plug, fits with
the lack of a highly fibrous cervix. So this rodent has diverged from others
in a whole suite of coadapted anatomical features of the lower regions of
the male and female reproductive tracts, and some of these features, at
least, relate to a unique type of copulation. Interestingly, such adaptations
may have disadvantages. The female tract is perhaps poorly adapted for giving
birth, as we have found many animals that have died with the fetus only
partially expelled through the cervix.

A few years ago, researchers studying primates suggested that the size
of testis and number of sperm relate to the mating system. Where more than
one male mates with a female at oestrus, sperm from different males may
compete for access to unfertilised eggs with the female’s reproductive tract.
This ‘sperm competition’ might maximise the number of sperm produced and
hence the evolution of relatively large testes. Conversely, in species that
are monogamous or breed in single-male groups, there would be less competition
between the sperm of different males, and so testes should tend to be smaller
and produce fewer sperm.

On the basis of its reproductive anatomy, the hopping mouse would seem
to fall into the less competitive group. But does it? In the early 1970s,
Meredith Happold at Monash University in Melbourne compared the behaviour
of several species of rodents, including the spinifex hopping mice. She
described four types of social organisation, with the hopping mouse at one
end of the spectrum. When she placed strangers of this species together
there was some initial aggression, but soon all the hopping mice huddled
together in the group. When she tested single adult males and females in
a neutral arena, the female was usually the more aggressive sex. Similarly,
if she placed two strange males together, they generally showed far fewer
aggressive interactions than did two females, regardless of the stage of
the oestrous cycle. We repeated these studies, with the same results. Also,
when pairing up animals in our breeding colony, we found a small number
of adults dead within 24 hours. Almost always, it was the male that was
killed by the female, hardly ever the reverse.

Most researchers assume that, in mammals, aggression is stimulated by
the secretion of testosterone from the testes. So we measured levels of
this hormone circulating in the blood of animals of both sexes. We found
that, even though adult males were less aggressive than females, they usually
have higher levels of androgen in their blood. Testosterone is also the
classic ‘anabolic steroid’, leading to a bigger body size in males. Yet
when we matched adult male hopping mice to females of the same age, we found
that females often tended to be slightly heavier than males – which could
perhaps be linked to their greater aggressiveness. The general rule that
androgens make male mammals more aggressive and heavier than females does
not hold true for hopping mice.

To return to the animal’s breeding system and social organisation: what
happens in the natural environment? The short answer is that we still do
not know. The fact that groups of strangers of both sexes huddle together
within a few hours of being placed in one cage seems to suggest that in
the wild they do not usually live as single pairs or as breeding units with
a single male. This presents an apparent dilemma: males have small testes
but do not seem to live in single-male breeding groups. The explanation
could be that the small testes reflect lower levels of sperm competition
between cohabiting males due to the greater aggressiveness of the female.
It may be that once a female has been mated by one of the males within the
group she will prevent other males from mating with her. This would greatly
reduce the chances of sperm competition.

In a series of experiments with Mark Adams and Peter Baverstock of the
South Australian Museum, we screened our colony of hopping mice and found
genetic markers that could distinguish the offspring of particular males.
Out of more than 20 litters born to the female hopping mice kept with two
males, not one litter showed evidence of multiple paternity, although the
female sometimes switched from one male to the other in successive mating
periods. The findings are consistent with our theory that the female will
mate with only one male at any one oestrus, although we still need more
observations to confirm this.

We also need to determine why this species of murid rodent, living in
the sands of central and western Australia, has such a peculiar reproductive
anatomy. Most perplexing of all, perhaps, is what might have led to the
evolution of these divergent structures. Several other murids of the arid
zone of Australia have larger testes and a conventional sexual anatomy.
Nor are small testes necessarily associated with hopping, as kangaroo rats
of North America and jerboas and gerbils of Africa and Asia usually have
large testes and conventional reproductive tracts. Comparative field studies
may throw light on this conundrum, but these are hampered by the inaccessibility
of the animals’ natural habitat. These mice remain a challenge for mammalogists
keen to further our knowledge of the native rodents of Australia.

Dr W. G. Breed lectures in comparative anatomy and histology at the
University of Adelaide in Australia.