From a human perspective, sexes seem a relatively simple thing to get one's head
around—there are females, and there are males. But our perspective seems biased and narrow
when applied to life as a whole, says evolutionary biologist Laurence Hurst of the
University of Bath, United Kingdom.“If you were a single-celled alga sitting in a pond, you
wouldn't see the world as splitting into males and females.”
In fact, different species have evolved a bewildering number of ways to mix and match
the attributes of sexes. Some do not have males and females, but have adaptations that mean
each individual performs a specific role during sex. There are other species of which every
member is sexually equivalent, but individuals nevertheless divide into groups for the
purposes of mating. And in some species, individuals make both eggs and sperm (Box 1). This
biological diversity has produced a semantic muddle among biologists—everyone who thinks
about the evolution of sexes seems to have a slightly different take on what a sex is. “The
literature is highly confusing—we need to clarify our terminology,” comments Rolf Hoekstra,
a geneticist at the University of Waageningen in the Netherlands.
As things stand, there are three main aspects to the definition of a sex: who you are,
who you can mate with, and who your parents are. The third part of this trinity—parental
number—shows the least variation in nature. No known organism needs more than one mother
and one father. But even this assumption is now starting to break down at the level of
biological systems. In a recently discovered hybrid system within the harvester ant genus
Pogonomyrmex , queens must mate with two types of males to
produce both reproductive individuals and workers (Figure 3). These ants are the first
species known which truly has more than two sexes—with colonies effectively having three
parents— argues Joel Parker of the University of Lausanne, Switzerland.
Parker's ideas might reactivate evolutionary biologists' interest in sexes, which has
lain somewhat dormant since the 1990s. It could also provide a new route to experiments—
something often lacking in the field. Not everyone agrees that it makes sense to define the
ants' genetic quirks as new sexes. Each ant is still only a mix the genes from no more than
two parents, after all. But Parker believes that our current ideas about mating systems may
not be adequate to describe the ingenuity of evolution. “Until you see a three-sex system,
you don't know what it'll look like,” he says.
Little and Large
To address whether these ants have more than two sexes, we first need to look at other
candidates for sexes, their numbers in different species, and how these systems evolved.
One thing biologists do agree on is that males and females count as different sexes. And
they also agree that the main difference between the two is gamete size: males make lots of
small gametes—sperm in animals, pollen in plants—and females produce a few big eggs. But
researchers also think that before males and females evolved, sex occurred between
organisms with equal-sized gametes, a state called isogamy.
Evolutionarily speaking, an isogamous species faces two pressures. Individuals can make
more smaller gametes, thus increasing their potential number of offspring, or they can make
fewer bigger gametes, thus giving their offspring a better start in life by providing them
with more resources. Theoretical analyses suggest that this pressure is particularly great
if being big carries large benefits, making isogamy unstable. The original identical
gametes will evolve towards the opposite ends of the size spectrum.
In many species, however, one size of gamete still fits all. The organisms that have
hung on to isogamy are found among the less complex branches of life, such as fungi, algae,
and protozoa. This might be because large gametes, yielding well-funded zygotes, are likely
to be more strongly selected if the resulting offspring needs to grow into a large and
complex organism. The benefits of large gametes in simple and unicellular organisms are not
so obvious. Some support for this hypothesis comes from the algae belonging to the group
Volvocales. The variation in gamete size within each species matches its degree of
complexity. For example, the unicellular species
Chlamydomonas rheinhardtii is isogamous, while
Volvox rouseletti , which lives in balls of up to 50,000 cells,
has large and small gametes (Figure 4).
The Opposite of Sexes?
The question of sexes, and their number, is complex in isogamous species. Such species
still typically comprise different groups for mating purposes. They have genes that allow
them to mate with everyone except those belonging to the same “mating type” (this is
presumably to avoid inbreeding and to produce offspring that are genetically diverse to
cope with environmental change or biological enemies). Species with mating types, rather
than males and females, aren't limited to two interbreeding groups: the ciliate protozoan
Tetrahymena thermophila has seven, and the mushroom
Schizophyllum commune has more than 28,000, for example. Some
biologists call these mating types sexes; others think that, in the absence of traits other
than sexual compatibility or the lack thereof, it makes more sense to view species with
many mating types as having no sexes, rather than lots.
Yet most isogamous species have only two mating types. This seems perverse—it excludes
half the population as potential mates without gaining the benefits of specialization in
sexual biology. With William Hamilton, Hurst came up an explanation for this apparent
inefficiency.
Two-group mating systems, they proposed, evolved as a way for genes in the nucleus to
police the DNA in organelles. Cellular structures with their own genomes, such as
mitochondria and chloroplasts, can divide more rapidly than the cells that house them. If
the inheritance of organelles was biparental, selfish mutations in their DNA could spread
rapidly, Hurst and Hamilton showed. A nuclear gene that enforces uniparental inheritance of
organelles, along with a label that allows such cells to recognize each other so that their
nuclear genes can share the benefits of cytoplasmic policing, should be favored.
The mating biology of isogamous species offers considerable support for this idea. The
aforementioned
C. rheinhardtii , for example, comes in two mating types called
plus and minus. When the two fuse, the plastid of the minus cell is detroyed. Most
isogamous species that fuse cells have a similar mechanism. Male-killer parasites such as
Wolbachia , a parasite of arthropods, show the selection
pressure that intracellular passengers can exert (see also the primer by Wernegreen in the
March issue of
PLoS Biology ). And cellfusion experiments hint that biparental
inheritance of organelles does indeed cause problems, says Hurst. “Hybrids are often
rubbish, but they can be better if a drug is administered that inhibits the mitochondria of
one cell line.”
The species that have lots of mating types, such as ciliate protozoa, exchange nuclear
DNA, but not cytoplasm, and hence not intracellular organelles. Since individuals are freed
from the need to police their organelles or keep out parasites, selection favors the widest
assortment of possible mates, and thus the evolution of a large number of mating types so
that one's own type—which one can't mate with—is a small subset of the population. It is
possible to imagine species with cytoplasmic policing likewise having many mating types,
but such a situation would be much more prone to break down and be invaded by selfish
agents than one with two clearly defined types, which is what we usually see in nature.
Some have argued that cytoplasmic policing might also be a selective force for
different-sized gametes. Sperm could be small so that they do not import mitochondria into
the egg.
More than a decade after he devised it, Hurst's is still the leading hypothesis
explaining the number of mating types in a species. But experimental evidence remains
frustratingly elusive. “I wouldn't say I was entirely satisfied,” says Hurst. “We've got
all these ideas, and they turn out to be quite hard to test—there's no simple thing one can
do on a single species.” There are species where the uniparental inheritance of organelles
is not so strictly enforced, says Hoekstra, such as yeasts and plants. “It's not easy to
see if selection [on organelles] is strong enough,” he says.
Three's Company
Yet even in a species such as
S. commune , with its thousands of mating types, each sexual
encounter involves only two cells. Nor are we likely to find a species that defies this
pattern. The technical difficulties of combining more than two sets of genetic information
into one individual, and of parceling out that information during meiosis, must be vast,
says Brian Charlesworth of the University of Edinburgh. “We've reached the point of two
cells fusing, and stuck with that; two cells are probably just as good as three,” he
says.
The ant colonies that Parker suggests have three parents are a hybrid of the species
Pogonomyrmex rugosus and
P. barbatus . The hybrids have not yet been classed as a new
species, but they are well established across the southwestern United States, and there is
no evidence of contemporary gene flow between hybrids and their parent species.
Each ant has one parent if it is male, because male ants are produced from unfertilized
eggs, or two if it is female. But each sex also comes in two genetic strains. If a queen
mates with a male of her own strain, her offspring will be queens, and if she mates with a
male from the other strain, the sperm will give rise to workers. So, for a colony to
function fully it—and the queens it produces, because workers raise queens—must have two
fathers and one mother. And if any one group were to disappear, the population as a whole
would go extinct—unlike fungal mating types, where it's easy to imagine that the species
would carry on if a few disappeared. “If you lose any one, the whole thing collapses,” says
Parker. “It's really different from any other system.”
So, Parker argues,
Pogonomyrmex has four sexes: the males and females of each
strain. The idea is particularly potent if one views a social insect colony as a
“superorganism,” with the workers equivalent to the cells of a body. It's as if a female
mates with one male to produce her offspring's somatic cells, and another to produce its
germ cells. The ants form chaotic mating swarms, so most queens have no problem mating
multiply and getting sperm from males of both strains, although one would expect that males
would strongly favor mating with females of their own strain.
It's not known how the system originated. Separating the worker and reproductive castes
by genetics—other social insects do this by environment, that is, by rearing workers and
reproductives differently—may allow selection to operate more efficiently on each lineage,
and the workers may benefit from hybrid vigor: field researchers report them as being
highly aggressive. In an echo of Hurst's hypothesis, the system also mixes mitochondrial
and nuclear genes differently in queens and workers.
Some evolutionary biologists, such as Charlesworth, do not consider
Pogonomyrmex '
s mating types sexes, arguing that to define sexes in yet another way
only confuses the picture further. “[The ants] are an interesting system, but I wasn't
persuaded by Parker's interpretation,” Charlesworth says. “I'm not a fan of the idea that
it's useful to use the word ‘sex’ to describe compatibility between mating types—it muddies
the waters.” Others are more positive towards Parker's interpretation: “It deserves to be
taken seriously,” says evolutionary biologist Eörs Szathmáry of the Collegium Budapest in
Hungary. “He's thrown a stone in the water—now we need to see what kinds of ripples it
makes. You can't falsify a definition in the way you can a hypothesis; what determines
their fate is whether people find them useful or not.”
Species in which some individuals give up their reproductive opportunities to form part
of a breeding group, such as slime molds, might have a system similar to that of the ants,
Parker believes. “There may be hidden mating incompatibilities,” he says. “Now [that]
people know to look, we're going to start seeing more of these systems.”
