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To survive as a predator in the cold, dark depths of the ocean is not
easy. For a carnivorous fish, the laws of ecology and probability conspire
to make it hard to find both prey and potential mates. Angler fish, a group
of deep-sea fish, have solved both problems in unusual ways. Instead of
hunting, angler fish lure prey with a special luminescent ‘bulb’, fashioned
from a ray of the dorsal fin. Their method of finding a mate is even more
bizarre. According to popular theory, male and female angler fish pair bond
for life, the male reduced to a tiny blob of testis attached to the female’s
body and nourished by her blood. When the time for breeding comes, both
the host female and parasitic male can be assured that sperm and eggs will
be available. The problem of finding a mate is solved.

The reality is, intriguingly, even more complex. In some species of
angler fish, males probably do derive nourishment from their partners, as
both female and male blood systems form extensive, intertwining sinuses
in the areas, much as in the placenta. But as Theodore Pietsch of the University
of Washington has discovered, in other species males attach onto females
only briefly, leaving to resume a free-swimming existence. Males of all
species must be free-swimming at some time, and their well-developed olfactory
organs suggest that they find females largely by smell. With their big nostrils
and teeth modified to form a pincer-like attachment organ, free-living males
look so different from females that many early ichthyologists described
them as separate species.

The reproductive strategy of the deep-sea angler fish may well be unique
for a vertebrate, but parallels can be found in animals without backbones.
All can be lumped together as instances of ‘dwarf males’ where tiny males
are for brief periods at least attached to females of the same species.
If males feed off the female, they are sometimes little more than a huge
testis. Yet I hesitate to call such males parasitic, because most biologists
use the term to describe interactions between, not within, species. In addition,
parasitism is a one-sided, exploitative relationship in which the parasite
harms its host. In cases where dwarf males trade sperm for nutrients, both
partners obtain some benefit from the association.

Dwarf males have been discovered in a variety of invertebrate groups,
including certain flatworms, rotifers, nematodes, annelids, echiuroids,
crustaceans and molluscs. Details of the biology of dwarf males in a bivalve
mollusc were provided recently by Marcella Pascual and her colleagues at
the Institute of Marine Biology and Fisheries in Argentina. They found that
in the flat oyster Ostrea puelchana, larger individuals are usually female
and smaller ones male. Large females often carry the very smallest males
on their shells. Male oysters are attracted to females during their laval
stage, and settle to become dwarf males. In one experiment, Pascual showed
that females actually retard the growth of dwarf males, and that these males
may be older than free-living males of the same size.

Species that have dwarf males have something in common: something about
their lifestyle makes it hard to find a mate. Angler fish live a sedentary
life, and so do the flat oysters and the burrowing barnacles, which Darwin
noted also sport dwarf males. Many of the flatworms and nematodes with dwarf
males are parasitic, living at relatively low densities within the bodies
of their hosts. Another bivalve mollusc, the shipworm Zachsia, lives in
burrows at low densities among the root-like structures of clumps of sea
grass, while the bivalve Pseudopythinia often lives attached to crustaceans,
and has a scattered distribution forced upon it by the territorial habits
of its crustacean hosts.

But the example of the flat oyster introduces another twist to the tale
of dwarf males. In many invertebrate species with dwarf males, especially
bivalve molluscs, individual organisms can change sex during their lives.
Most of these species start their lives as sperm-producing males and then
switch to egg-producing females as they grow large. Michael Ghiselin of
the California Academy of Science suggests that such sex change should be
favoured by natural selection when an individual’s ability to reproduce
successfully as a male or female changes with age or size. Ghiselin also
argues that one sex must benefit reproductively from large size more than
the other sex. Models developed by Eric Charnov of the University of Utah
confirm Ghiselin’s idea. In the case of flat oysters – which are male first,
then female – Ghiselin’s theory predicts that large size should be more
crucial to success for females than for males. In many invertebrates, and
some vertebrates, too, larger females produce more or larger eggs than smaller
ones, which is a clear advantage.

Males that need not fight

But what about dwarf males? Biologists often assume that being big is
always advantageous in males. Charles Darwin introduced this idea in his
book The Descent of Man and Selection in Relation to Sex, published in 1871.
Darwin stressed that, in the struggle among males to obtain matings, the
evolution of weapons and large body size should be favoured by the process
he termed sexual selection. Bigger and stronger males should acquire more
mates than their smaller and weaker competitors. But in certain cases, as
when animals live widely scattered, aggressive competition among males for
mates will be rare, and so sexual selection for larger males will be reduced
if not absent. Ghiselin argues that, under this circumstance, selection
may place a premium on a very different sexual strategy in which a male
matures early (when still small) and then speedily searches for a female,
settling as a dwarf male once a partner is found. Ghiselin described this
race to reproduce as a strategy of ‘first come, first service’. In some
angler fish, this strategy of speedy development has resulted in such an
early maturation of the male reproductive system that certain other organ
systems remain in a larval or juvenile state. Stephen Gould of Harvard University
has coined the term ‘heterochrony’ to describe such evolutionary changes
in the timing of development such that individuals display mosaics of immature
and adult characteristics.

Once settled in or on a female, the dwarf male is in a position to release
sperm when fertilisation is most likely. In flat oysters, a dwarf male is
most likely to settle with his exhalant siphon, from which sperm are released,
positioned near the female’s inhalant siphon. Water currents then carry
sperm into the female’s inhalant siphon, and fertilisation happens within
her body. For those angler fish species in which the male receives nutrients
from his partner’s circulation, blood-borne hormones secreted by the female’s
pituitary gland might synchronise his reproductive physiology with hers.
Such a close relationship has led Leo Demski of the University of Kentucky
to suggest that the reproductive pattern of these angler fish represents
a strange kind of acquired hermaphroditism, in which the female host acquires
male reproductive function. In a number of species, including some angler
fish and many bivalve molluscs, more than one dwarf male may be associated
with a single female. From the female’s perspective this situation can only
further increase the likelihood of successful fertilisation. For the males
it may result in competition for opportunities to fertilise their host’s
eggs. Presumably, the male who is in the best location and who releases
the most sperm at just the right time wins, fertilising the most eggs.

The fate of dwarf males in the longer term varies enormously. In species
where they hook onto females permanently, such as the barnacle Trypetesa
which burrows into snail shells, dwarf males may lose all of their internal
organs except the testis and associated structures. In the angler fish,
males may form only temporary associations with females, presumably leaving
after spawning to search for other mating opportunities. From Ghiselin’s
theory we can predict that population densities, and thus male-female encounter
rates, will be higher in those angler fish species in which males leave
females than in those in which males attach permanently. In the flat oyster,
dwarf males seem to become less common as the density of the population
increases, perhaps because it is then easier for sperm to find eggs. For
those invertebrate species with sex changes as well as dwarf males, such
as Pseudopythinia, males may associate with females only temporarily, leaving
as they get larger to live for a time as free-living males and later, as
they grow even more, to turn into females.

Many interesting questions remain to be answered. For example, should
a dwarf male flat oyster remain with a female (and a predictable supply
of eggs to fertilise) or leave her in an attempt to grow and become female
himself? The answer may lie in the probability of the male becoming larger
than his partner when he adopts a female function himself. If the male could
produce more eggs as a female than his partner and if he could acquire enough
sperm to fertilise these eggs, then perhaps he should leave, grow and change
sex. A rather different type of question may be asked about the dwarf male-female
relationship in certain angler fish. What immunological features enable
the females of some species to accept ‘non-self’ male tissue without rejection?
An answer to this question could contribute to our understanding of transplant
immunology.

Getting sperm and eggs together is a problem in many animal groups.
An individual searching or advertising for a mate uses up lots of energy,
and is exposed to the dangers of parasites and predators. Similar dangers
can befall sperm as they search for eggs to fertilise. This problem is likely
to be especially acute in organisms living at low population densities,
where, in addition to all of these other problems, encounters between males
and females or sperm and eggs may be rather infrequent events. It is then
that dwarf males may be most likely to succeed in the struggle to reproduce.

* * *

When does it make sense to change sex?

Changing from one sex to the other as an individual grows larger and
older is known as sequential hermaphroditism. Michael Ghiselin believes
that this peculiar phenomenon can evolve when one sex benefits more than
the other from being big.

Ghiselin’s idea is illustrated in two graphs plotting the numbers of
offspring produced by males and females against body size. In both graphs,
larger individuals of both sexes produce more offspring. But in Figure 1,
the male benefits more than the female by being big. Under this situation,
an individual may produce the most offspring if it reproduces as a female
when small and then switches to male function when larger. This pattern
of sex change is called protogynous (or female-first) hermaphroditism. In
Figure 2, both sexes again benefit from larger size but in this case the
benefit to females is disproportionately greater than that to males. It
may pay to function as a male when small and switch to being female as body
size increases, a pattern of sex change known as protandrous (male-first)
hermaphroditism.

Coral reef fishes provide some of the best-studied examples of sequential
hermaphroditism in animals. The largest individuals in groups of blue-headed
wrasses, Thalassoma bifasciatum, usually are male. On small reefs, males
compete for harems of females and a single, successful male may control
access to all of the females on his reef. So for males there is a clear
advantage to being large, and this wrasse exhibits protogynous hermaphroditism.
If the harem master is removed from his reef, the largest fish in the harem
will then change sex from female to male to replace him. The clownfish Amphiprion
akallopisos is a protandrous hermaphrodite and lives as monogamous pairs
around sea anemones. The number of offspring a pair can produce is limited
by availability of eggs, and larger females produce more eggs than smaller
females. Not surprisingly, in pairs of clownfish, the larger individual
is female. But if the female of a pair is removed and replaced with a fish
smaller than the male of the pair, the latter will change sex to become
an egg producer.

Situations in which one sex benefits more than the other from being
big are common throughout the animal kingdom, but sex change, though widespread,
is really quite rare. Among the vertebrates, for example, sex change is
not found in reptiles, birds or mammals; it may occur in a few amphibians.
Eric Charnov of the University of Utah offers several reasons why sex change
is not more common. He points out that there may be costs to changing sex
that outweigh benefits, such as temporary loss of breeding opportunities
or increased risk of dying. In some animals, the developmental and anatomical
specialisations associated with function as either a male or a female may
be so great that changing from one sex to the other is simply biologically
impossible.

* * *

A formative experience for dwarf male worms

Perhaps the best-known example of dwarf males in the invertebrates is
found in a curious phylum of worms known as the Echiura. This group is composed
largely of bottom-dwelling, detritus-eating animals which probably are most
closely related to the segmented annelids (a group which includes the familiar
earthworm and lugworm). In at least one echiuran family, the Bonellidae,
males are reduced to mere dwarfs.

The best-studied species, Bonellia viridis, is found throughout the
Mediterranean. Female Bonellia are truly sedentary and rather cryptic animals,
often occupying ducts and galleries formed by boring molluscs. The cylindrical
body of the female is between 5 and 12 centimetres long and ends in a thin,
extendable proboscis which is used to nose around the substrate in search
of food. When fully stretched, the proboscis may be over 1 metre long. Eggs
produced by females hatch into tiny larvae, and whether a larva becomes
male or female depends largely on the environment it encounters. For the
most part, larvae differentiate into females in the absence of adults of
the same sex but become males if they contact other females.

In contrast to females, male Bonellia are tiny, seldom reaching more
than about 3 centimetres in length. When a larva encounters and attaches
to the body of a female, using a muscular sucker, its organ systems such
as the gut either fail to develop beyond the larval state or simply degenerate,
as do the sensory eyespots. The muscular attachment organ gradually disappears
and, after about one week, the tiny worm migrates through the gut of the
female to take up residence close to her oviduct. With little more than
its reproductive and excretory systems functional at this time, the dwarf
male presumably is in a prime position to fertilise his host’s eggs.

Despite a great deal of interest throughout this century, our understanding
of the exact manner by which contact with a female masculinises a larval
Bonellia has long been confused. For many years, it was believed that the
green integumentary pigment of females played a critical role in the process.
This pigment, known as bonellin, is actually toxic. Laboratory tests have
shown that it kills cancerous cells and, at high concentrations, even kills
Bonellia larvae. Recent experiments by V. Jaccarini and colleagues at the
University of Malta have provided some interesting new information on this
subject. They exposed undifferentiated larvae to different types of extracts
from females in laboratory cultures. As expected from the results of the
older research, introducing extracts of the female proboscis and trunk meant
that most larvae became male. However, the pigment bonellin resulted in
fewer larvae becoming male than the general extract, indicating that some
other chemical substance must also play an important role. Most larvae exposed
to pure seawater differentiated into females.

The story then gets more complex. Jaccarini found that some larvae,
exposed to female extracts, became females themselves, contrary to the general
pattern. In addition, some larvae exposed simply to pure sea water became
male, another unpredicted result. Assuming that Jaccarini’s experimental
cultures were uncontaminated, these findings suggest that there may be some
genetic control of sex determination in Bonellia, but that it can be overridden
by the more prevalent process of environmental control.

Another surprising finding was that, in the laboratory, larvae sometimes
interacted with one another, one assuming a female role and the other differentiating
into a dwarf male. It seems unlikely that anyone will be able to study the
reproductive tactics of Bonellia in its natural environment. But it may
be that larvae are programmed to decide where they settle on the basis of
such factors as density of individuals and the sex ratio in the area.

Paul Verrell is an ethologist at the University of Chicago.