NEWS & VIEWS NATURE|Vol 451|3 January 2008

ranging from habitat destruction to are often contentious and difficult

BLICKWINKEL/HARTL

the effects of using wild fish to feed to implement, but ultimately they
farmed stocks4 become of greater can work. Similarly, the problems
concern. The emphasis of aquacul- facing the aquaculture industry
ture development has, not surpris- are not unsolvable, but denial that
ingly, been on increasing production, those problems exist will not pro-
lowering costs and improving prod- vide answers. In the case of salmon
ucts. These needs of the industry lice, solutions include adhering to
have been well served by the sci- strict guidelines on the introduc-
ence of fish farming. Unfortunately, tion and transfer of non-native
however, research pointing out the fish, and siting of net pens away
environmental costs of production from areas where wild stock is
has been viewed as an attack on the vulnerable. Overall, the priority in
industry, rather than as a challenge to aquaculture should be to anticipate
be tackled and overcome. any adverse environmental con-
Krkošek et al.3 have provided new, Figure 1 | Salmon louse. This marine organism belongs to a group of sequences and to tackle them at
empirical evidence of the environ- crustaceans known as copepods. It feeds on the external surfaces of fish, that stage, rather than struggle to
mental costs of the nearshore, net- and can eventually kill them. recover after those consequences
pen aquaculture of salmon — the are already apparent. ■
pending extinction of several populations of disease and parasite transmission, and other Andrew A. Rosenberg is at the Institute for the
wild pink salmon, Oncorhynchus gorbuscha, impacts will certainly apply to these species too. Study of Earth, Oceans and Space, University
on the coast of British Columbia. Until now, It is vital to assess the potential environmental of New Hampshire, Durham, New Hampshire
most research on the effects of net-pen aquac- costs and to reduce them before the advent of 03824-3525, USA.
ulture has revealed instances of certain conse- large-scale farming of these species. e-mail: andy.rosenberg@unh.edu
quences, such as the competition of wild fish Can we design aquaculture systems that
with escaped farm stocks for spawning habi- reduce ecosystem impacts, or eliminate some 1. Watson, R. & Pauly, D. Nature 414, 534–536 (2001).
tat, but not of effects at the population level. of them entirely? I think that we can, but not 2. Food & Agriculture Organization of the United Nations
State of World Aquaculture 2006 Fisheries Tech. Pap. 500
Krkošek and colleagues’ analysis of 142 popu- with a confrontational mentality. Overfishing (FAO, Rome, 2006).
lations of pink salmon shows that wild stocks of wild stocks is not a contrived problem, nor 3. Krkošek, M. et al. Science 318, 1772–1775 (2007).
adjacent to fish farms have suffered dramatic is it unsolvable: good management practices 4. Naylor, R. L. et al. Issues Ecol. No. 8 (2001).
increases in mortality of juvenile fish owing to
infestation by sea lice, Lepeophtheirus salmonis
(Fig. 1), and that most of the exposed popu-
lations are at risk of extinction within four NEUROSCIENCE
salmon generations. It is the location of the
salmon farms, compounded with the tendency
of sea lice to proliferate near intensive farm
Love hangover
facilities, that are cause for concern. Although
farmed salmon can be treated to reduce sea-
Leslie C. Griffith
lice infestation, wild stocks have no such pro- In many species, males have developed strategies to safeguard their
tection. As juvenile wild salmon emerge from
rivers, their migration route runs a gauntlet of
genetic material from dilution by that of competing males. Fruitflies achieve
salmon aquaculture pens and, therefore, high this by altering the behaviour of their partners.
levels of salmon lice.
The lesson of this analysis3 is that neither Sex can be transformative. Humans often tract, increasing the probability of successful
fisheries science nor the aquaculture industry romanticize the after-effects of copulation, but fertilization and implantation2. This type of
can be driven solely by the desire to increase for most organisms there are real biological post-copulatory effect benefits both the male
production. Many aquaculture facilities are consequences to mating that go beyond the and female partner. For many species there are
set in complex ecosystems, and influence the transfer of sperm. Most species have strategies also other mating-associated events that appar-
structure and function of those ecosystems. for protecting their genetic investment that ently maximize the reproductive success of just
Policy-makers must ensure that the environ- can involve alterations in both the biology and one of the involved parties, often at the expense
mental costs are evaluated and monitored, and behaviour of the mating partners. For example, of the other. An obvious example of this is mate
are factored into decisions about farm location in the fruitfly Drosophila melanogaster a com- guarding. Males of many avian, reptile, rodent,
and expansion. The argument that costs will be ponent of seminal fluid, known as sex peptide, primate and insect species remain close to a
unfairly passed on to consumers rings hollow, leads to increased egg-laying by the mated recent conquest to lower the probability of her
because if such costs are not controlled, we the female and behavioural changes that reduce the re-mating with a more desirable male and so
public eventually bear them in their entirety. In likelihood of her re-mating. How sex peptide diluting or displacing their own sperm. The
such a circumstance, there is little incentive for triggers such a complex array of effects was female may benefit in terms of decreased pre-
producers to reduce environmental impacts. unknown. On page 33 of this issue, Yapici dation, but she loses any opportunity to better
The results of Krkošek and colleagues’ study, et al.1 identify the receptor for sex peptide and the genetic lot of her offspring. The success
and their warning that the terrible cost of show that it is expressed in the reproductive of this strategy for the male depends on
extinction of wild-salmon stocks is not far off, tract and in a subset of female neurons believed his vigilance, and potentially decreases his
highlights that point. to be involved in sexual behaviour. chances of mating with other females, so is not
Net-pen aquaculture is not just about Enhancing the survival of potential progeny without cost.
salmon. As the industry expands into other is a common goal of males in many species. In Nature has also come up with more subtle
species, such as cod, halibut and sablefish, mammals, intercourse changes the immuno- forms of mate guarding. In snakes3 and various
the same concerns over the location of farms, logical environment of the female reproductive insect species4–6, mating can lead to changes
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NATURE|Vol 451|3 January 2008
in the female pheromone profile that decrease
the attractiveness of mated females to subse-
quent suitors. Females’ behaviour can also be
modulated by mating. In rodents, exposure to
dominant-male pheromones induces a female
preference for dominant versus subordinate
males that may involve introduction of new
neurons into neural circuits7. Similarly, female
jewel wasps change their response to male
sex pheromones from attraction to aversion
after mating8, and in D. melanogaster mated
females will actively reject courtship, kicking
and running away from a new male9. This type
of ‘mate guarding’ does not require the contin-
ued presence of the successful male, maximiz-
ing his ability to mate with other females while
still protecting his DNA investment. Many of
these after-effects are generated by chemicals
produced by the male and transferred to the
female in his ejaculate.
The best-understood example of a behav-
iourally active seminal-fluid component is
sex peptide in D. melanogaster 9. It is produced
in the male accessory gland, a prostate-like
structure, and is absorbed into the female cir-
culation from the vaginal tract. Behaviours
resulting from sex-peptide absorption include
increased egg-laying and reduced receptivity to
male courtship. Previous studies indicated that
there are binding sites for sex peptide in the
brain9, but the nature of the receptor or recep-
tors was unknown.
To identify the receptor, Yapici et al.1 carried
out an RNA-interference-based genome-
wide screen for genes required in females for
post-copulatory behaviours; they reasoned
that genes whose reduced expression blocked
mating-induced increases in egg-laying would
be candidates. This approach identified a gene
for a putative G-protein-coupled receptor.
Reducing the expression of this gene did not
affect the receptivity of virgin females or sperm
storage in mated females, but it completely pre-
vented the development of post-copulatory
behaviours in either mated females or virgin
females injected with sex peptide.
To determine whether their candidate gene
was a bona fide sex-peptide receptor (SPR),
the authors expressed it in mammalian cells
maintained in culture. They found that sex
peptide and DUP99B — a seminal-fluid com-
ponent that can also mediate the switch to
mated-female behaviour — activate SPR with
nanomolar affinity. Other Drosophila neuro-
active peptides whose receptors are closely
related by sequence to SPR did not activate
it. SPR homologues from other drosophilids,
Bombyx mori and Aedes aegypti, also responded
robustly to sex peptide and DUP99B, indicat-
ing that SPR is not unique to D. melanogaster.
The distribution of SPR provides some clues
to how it might effect behavioural changes. The
authors demonstrate that SPR is present both
in the reproductive organs of the female and
on the plasma membranes of neurons close to
the surface of the central nervous system. Pre-
vious work by this group10 has suggested that
Drosophila neurons that express a putative tran-
scription factor encoded by the fruitless gene
are required for suppressing mated-female-
like rejection behaviours. Yapici et al. now
find that a subset of these neurons also express
SPR, implying that sex peptide modulates
these neurons. They used RNA interference to
decrease SPR expression in fruitless-express-
ing cells, and overexpressed SPR in mutant flies
that could not express it, to demonstrate that
expression of SPR in this subset of cells is both
necessary and sufficient for the development
of post-copulatory behaviour.
For students of neurobehaviour, the most
interesting finding of Yapici and colleagues’
study is that, in SPR, they now have another
specific molecular tag for cells involved in an
intriguing and ‘plastic’ behaviour, allowing
them to perform a complete analysis of this
behavioural circuit. The more global impact
of the work, however, is that it provides a new
target for the development of insect-control
compounds. That SPR-like receptors exist in
most sequenced insect genomes suggests that
antagonists of this receptor could be used to
reduce insect populations by blocking egg
maturation and extrusion, or perhaps SPR
agonists could be used to make virgin females
reject mating. Although the irony of having
their own weapon turned on them will doubt-
less be lost on the male insects, it is a satisfying
and potentially specific approach.
Another question raised by this work
is: how widespread is this type of ‘mating-
induced mind control’? At least one species of
vertebrate, the red-sided garter snake, dem-
onstrates mating-induced reductions in
NEWS & VIEWS
IMAGEBROKER/ALAMY
After mating, male fruitflies
don’t have to stand by and
guard their transferred genetic
material — sex peptide in their
semen will do the job.
female receptivity3. Obvious homologues of
sex peptide and SPR have not been identified
in vertebrates, but this is not surprising given
that genes involved in reproduction have a very
fast rate of evolution — precisely because they
are involved in reproductive behaviour — and
this variation promotes the differentiation of
species11. Although sequence mining has not
found much homology along the phylogenetic
tree, using more subtle algorithms to analyse
protein structure and function indicates that
there are fairly striking similarities between
components of Drosophila and vertebrate semi-
nal fluid12. Perhaps there is yet another reason
to use a condom, ladies. ■
Leslie C. Griffith is in the Department of Biology,
Volen Center for Complex Systems and the
National Center for Behavioral Genomics,
Brandeis University, 415 South Street, Waltham,
Massachusetts 02454-9110, USA.
e-mail: griffith@brandeis.edu
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33–37 (2008).
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3. Mendonca, M. T. & Crews, D. Horm. Behav. 40, 43–50
(2001).
4. Nagalakshmi, V. K., Applebaum, S. W., Azrielli, A. & Rafaeli,
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