Download Why are sexually selected weapons almost absent in females?

Current Zoology
59 (4): 564–568, 2013
Why are sexually selected weapons almost absent in females?
Anders BERGLUND*
Department of Ecology and Genetics/Animal Ecology, Uppsala University, Norbyv. 18d, 752 36 Uppsala, Sweden
Abstract In sex role reversed species, predominantly females evolve sexually selected traits, such as ornaments and/or weapons.
Female ornaments are common and their function well documented in many species, whether sex role reversed or not. However,
sexually selected female weapons seem totally absent except for small wing spurs in three jacana species, present in both males
and females. This poor female weaponry is in sharp contrast to the situation in species with conventional sex roles: males commonly have evolved sexually selected weapons as well as ornaments. At the same time, females in many taxa have naturally selected weapons, used in competition over resources or in predator defence. Why are sexually selected weapons then so rare, almost absent, in females? Here I briefly review weaponry in females and the function of these weapons, conclude that the near absence of sexually selected weapons begs an explanation, and suggest that costs of sexually selected weapons may exceed costs of
ornaments. Females are more constrained when evolving sexually selected traits compared to males, at least compared to those
males that do not provide direct benefits, as trait costs reduce a female’s fecundity. I suggest that this constraining trade-off between trait and fecundity restricts females to evolve ornaments but rarely weapons. The same may apply to paternally investing
males. Whether sexually selected weapons actually are more costly than sexually selected ornaments remains to be investigated
[Current Zoology 59 (4): 564–568, 2013].
Keywords
Sexual selection, Female weapons, Female ornaments, Sex role reversal
1 Introduction
Traits used as weapons in fights between individuals
are common in animals, and are found in both males
and females of many species (Emlen, 2009). Weapons
(for definitions, see Box 1) may serve functions in for
instance predator defence, defence against suitors, in
resource competition, or in mating competition. For
females, some additional explanations to weapon evolution have been suggested: they may exist due to a genetic correlation with the same trait in males (interestingly, the reverse has not been suggested, i.e., males
possessing weapons due to a genetic correlation with the
corresponding female trait). Moreover, another suggestion for the evolution of female weaponry, the male
mimicry hypothesis, is about avoiding intimidation of
sons by weapons in adult males – if the mother is also
armed, sons may be less scared by adult males and stay
with the mother for longer (Estes, 1991). So which of
these functions do female weapons serve? I will briefly
go through some well researched taxa, and discuss how
female weapons are used. I will not dwell on differences
between adaptive and non-adaptive (i.e., genetic correlations between the sexes) explanations, and I will not
try to differentiate between the explanations relying on
Received Mar. 10, 2013; accepted May 2, 2013.
∗ Corresponding author. E-mail: [email protected]
© 2013 Current Zoology
natural selection (e.g., anti-predator, resource defence,
male mimicry), but I will contrast natural selection explanations with sexual selection ones.
2
The Use of Female Weapons
In bovids (cattle, sheep, goats and antelopes) males
typically have horns, but in many species females also
possess such weapons, albeit usually smaller and differently shaped (Caro et al., 2003; Bro-Jørgensen, 2008;
Stankowitch and Caro, 2009). In male bovids, horn
evolution is thought to be driven by male-male competition for females, whereas female horns may serve as
defence against predators or in female-female competition over territories (Roberts, 1996; Stankowitch and
Caro, 2009). Indeed, horn size in females has been used
to quantify the proportion of male weaponry that can be
due to natural selection, the remainder is then assumed
to be sexually selected (Bro-Jørgensen, 2007). Large,
conspicuous, open-living bovids typically have females
with horns used in predator defence, and such horns are
thought to have evolved repeatedly in this family
(Stankowitch and Caro, 2009). In smaller, inconspicuous territorial bovids, such as many duikers, females
defend their territories against other females aided by
their horns. Horns of this type are thought to have
BERGLUND A: Sexually selected weapons in females
Box 1
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Vocabulary
•
Natural selection: a process by which biological traits become either more or less common in a population as a function
of the differential survival and reproduction of their bearers. Natural selection includes social and sexual selection, but
when I contrast natural with sexual selection in this paper I mean natural selection exempting sexual selection.
•
Social selection: a form of natural selection where selection stems from intraspecific social competition, both sexual and
non-sexual. Social selection thus includes sexual selection. My use of the term here should not be confused with ideas
unfortunately using the same vocabulary but refuting the process of sexual selection.
•
Sexual selection: “differences in reproductive success, caused by competition over mates, and related to the expression of
the trait” (Andersson, 1994, p. 7 lines 21–23). The word “mates” can be exchanged for “fertilisations” to include
post-copulatory processes. Sexual selection is part of social and natural selection.
•
Weapon: a trait used in direct fights between individuals over a resource.
•
Sexually selected weapon: a trait used in direct fights between individuals of the same sex over access to individuals of the
opposite sex for mating purposes.
•
Ornament: a sexually selected trait attractive to the opposite sex.
•
Sex role reversal: when females are the predominant competitors for mates.
•
Conventional sex role: when males are the predominant competitors for mates.
•
Non-investing male: a male that provides females with genes but no direct benefits for her or her offspring, such as paternal
care, security or nuptial gifts. •
Investing male: a male that provides females with genes and also direct benefits for her or her offspring, such as paternal
care, security or nuptial gifts evolved once, and then only among the duikers
(Stankowitch and Caro, 2009).
In cervids (deer), females have antlers in only one
species, the reindeer, but these are again thought to be
naturally selected. Females use them to establish dominance, in particular over males. In fact, females keep
their antlers for longer than males, thus securing feeding
sites for themselves and their calves (Espmark, 1964).
Other ruminants also seem to lack sexually selected
weapons (Box 1) in females: ossicones (horn-like skincovered protuberances) in giraffes are used in malemale “necking” fights, whereas females have proportionately smaller ossicones, skulls and necks and are not
known to use them in combat or dominance (Simmons
and Scheepers, 1996). In the related okapi, however,
females are territorial (Hart, 1992) and may use their
ossicones in territory defence against other females. In
pronghorns, finally, female have pronghorns but presently seem not to use them at all, although these horns
have been suggested to be anti-predator devices against
now extinct predators (Byers, 1999). Thus, in no ruminant species females are known to use their horns in
intrasexual combat over males, presumably because sex
role reversal (Box 1) seems absent in this taxon.
The lack of sexually selected weapons in females
seems in fact to be the rule in all mammals. For instance,
in boars, elephants and rhinos females use tusks and
horns as tools or anti-predator devices, i.e. these traits
are naturally selected or due to a genetic correlation
with male traits (Estes, 1991). In male narwhales tusks
may be used in aggressive encounters (Silverman and
Dunbar, 1980). Some females may also develop tusks,
but their function, if any, is unknown.
Birds pose a much more interesting taxon for the
search for female sexually selected weapons. Several
sex role reversed species exist, especially among waders
such as phalaropes and jacanas. Unfortunately birds are
seldom heavily armoured, but spurs exist in many species. In three species of jacana, the wattled, the northern
and the pheasant-tailed jacana, males as well as females
have wing spurs (Fig. 1, Rand, 1954). They are similar
in size between sexes (Rand, 1954), but as females
overall are larger than males, spurs are proportionately
smaller in females. Nevertheless, females may use their
spurs in displays at mating time, “as if they were attempting to strike each other with their sharp spurs”
(Rand, 1954). These spurs are, in fact, the only (likely)
sexually selected female weapon I have found, even if
the evidence is somewhat anecdotal.
In several species of swans, geese, screamers, plovers
and lapwings both sexes may have wing spurs (Rand,
1954), but their function in females is not well known.
As these birds typically have more conventional sex
roles (Box 1) female spurs are unlikely to be used in
female-female fights over males, and their use seems
primarily to be defence against enemies or intruders
(Rand, 1954), or use in competition over resources for
chicks (B. Lyon, pers. comm.). Female rallids (coots,
moorhens) have huge claws (as do males), used in fights
over territory borders and resources for chicks (B. Lyon,
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Current Zoology
Fig. 1 A female northern jacana Jacana spinosa, with
wing spur
(from http://scienceblogs.com/tetrapodzoology/2010/07/14/spursblades-jacanas-lapwings/)
pers. comm.). The spurs in gallinaceous birds (fowl),
located on the tarsus, are found in males only (Rand,
1954).
In some reptiles, for instance horned lizards
(Phrynosoma) and thorny devils Moloch horridus, both
males and females have spiny horns (Emlen, 2008), but
these function primarily in predator defence (Young et
al., 2004). In fish sexually selected weapons are quite
rare, and I know of no case where females possess such
in spite of sex role reversal being not uncommon (e.g.,
many pipefish species, Berglund and Rosenqvist, 2003).
In some crustaceans females are armed, like in the
snapping shrimp Alpheus armatus, but those weapons
are used in territory defence (Knowlton and Keller,
1982). In several beetles females possess weapons,
sometimes even larger than those in males. This is for
instance the case in the dung beetle Onthophagus sagittarius, but these females use their horns in contests over
dung (a resource for reproduction), not in fights over
access to males (Watson and Simmons, 2010).
3
Why Are Sexually Selected
Weapons So Rare in Females?
Female sexually selected weaponry thus seems al-
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No. 4
most non-existent. Rather, when females possess weapons, they are naturally selected, used in competition
over resources other than mates, in predator defence, or
are non-functional (Caro et al., 2003; Bro-Jørgensen,
2007; Emlen, 2008). In other words, female weapons
may often belong to the realm of social selection
(West-Eberhard, 1983; Lyon and Montgomerie, 2012;
Tobias et al., 2012), but not to that of sexual selection as
defined in Box 1. Still, females in many species have
sexually selected ornaments, attractive to males (e.g.,
Clutton-Brock, 2009). Even if the endeavour to explain
the lack of something may seem strange, I still think the
paucity of female sexually selected weaponry, in the
face of frequent female ornamentation, begs an explanation. The question is then, why do females have ornaments, but typically not weapons, to aid them in acquiring males? One possibility is of course if weaponry and
sex role reversal for some reason are found in different
taxa – if so, females would remain unarmed in the context of sexual selection. This is perhaps a possibility in
mammals where sex role reversal is uncommon (but see
e.g. Kuester and Paul (1996) for a possible exception),
but cannot apply to birds, fish or insects, where we find
both sexually selected weapons and sex role reversal
within lineages. Another possibility is that females, for
some reason, engage in mate attraction and in dominance interactions, but not in direct fights with other
females over males. If so, sexually selected weapons
would of course be superfluous in females. However,
females of many species are indeed aggressive towards
one another and do engage in direct fights over resources as well as mates (e.g., Andersson, 1994; Eens
and Pinxten, 2000; Clutton-Brock, 2012).
To take one step back, we first need to understand if
costs and benefits of sexual selection differ between
males and females. If we compare non-investing males
(Box 1), who do not provide females or offspring with
direct benefits such as paternal care or nuptial gifts, with
females, sexual selection definitely operates differently
in the two sexes. In addition to all possible costs associated with developing and possessing sexually selected
traits that apply to both sexes, females always face an
additional cost: that to their fecundity. Resources allocated to a sexually selected trait will trade off with resources allocated to egg production in all females, and
also to any further offspring care if provided. This will
constrain the evolution of sexually selected traits in females: they need to trade ornaments for offspring (Fitzpatrick el al., 1995; Clutton-Brock, 2009; Tobias et al.,
2012). Exactly the same trade-off will be present in
BERGLUND A: Sexually selected weapons in females
males, if they provide females or offspring with direct
benefits (Fitzpatrick et al., 1995). In other words, anisogamy suffices to constrain trait evolution more in females than in males, and any further parental investment
(sensu Trivers, 1972) provided for the offspring by the
females may amplify the constraint. Conversely, a reversal in the difference of the direct benefits provided
by the parents, so that male parental investment exceeds
that of females, may reverse the constraint on trait evolution to operate more strongly on males. Still, even
under the last scenario, females will always produce
eggs, and so never can rid themselves from the trade-off
between fecundity and sexually selected traits. Moreover, benefits from sexually selected traits may also
differ between the sexes. Payoffs from such traits may
be lower in females than in males if for instance anisogamy thwarts the value of additional matings more in
females than in males. Again, this would act to produce
less extreme traits in females.
So, can this constraint on trait evolution in females
explain why they evolve ornaments rather than weapons?
Possibly, but only if sexually selected weapons are more
costly than ornaments. We expect females to evolve
“cheap” traits so as not to compromise their fecundity,
and if weapons are more expensive than ornaments that
would explain the paucity of the former. So are weapons
expensive? This is not known and for now remains a
speculation. I think it would be odd if energetic or other
production costs of weapons were prohibitive, as many
females possess naturally selected weapons. Can the
cost of provoking and entering real fights with other
females, risking injury, be prohibitive? If this is the case
costs and benefits from sexually selected traits could
look like in Fig. 2. Here, a steep rise in costs with trait
size for sexually selected weapons compared to ornaments, together with females being more cost-sensitive
Fig. 2 Possible benefits and costs with sexually selected
weapons and ornaments to females and non-investing
males
567
than non-investing males, prohibits females from
evolving weapons but permits the evolution of ornaments. Maximizing the difference between benefits and
costs in Fig. 2 would render sexually selected weapons
in females unfeasible, in contrast to male sexually selected weapons and male and female ornaments. A
similar argument could be raised when comparing investing with non-investing males (Box 1): we would
expect sexually selected weapons in the former to be
absent or small, and ornaments to prevail, i.e., the cost
curves in Fig. 2 may look similar for females and investing males. For simplicity the benefit curve in Fig. 2
is drawn similarly for females and non-investing males.
However, benefits may likely be lower in females if
they typically gain less from multiple matings compared
to males. Again, this would further reduce the likelihood
that females develop sexually selected weapons.
4
Conclusion and Future Directions
Sexually selected weapons in females are near-absent,
but female ornaments are not uncommon. As the evolution of sexually selected traits in females is compromised by effects to their fecundity, females are typically
very cost-sensitive. If sexually selected weapons somehow are more costly that ornaments, this may explain
the paucity of weapons in females relative to males. We
now need to understand several things to explain the
absence of female sexually selected weapons. First, we
need more clearly to understand the function of female
weapons. It is not uncommon to find explanations to
weapons in terms of their value to females in defending
resources for themselves and their offspring, but when
males have the same weapons and defend the same resources they are said do so to attract females. Thus, female weapons would automatically become “naturally
selected” and male weapons “sexually selected”! To
avoid such just-so stories we need much better insights
into how and why weapons are used. Second, we need
to compare costs of sexually selected weapons and ornaments. This may not be an easy task – often one and
the same trait functions as both a weapon and an ornament (Berglund et al., 1996), so disentangling the two
may be a formidable task. Moreover, costs must be
measured in terms of costs to individual fitness, and
such measures are notoriously difficult to obtain. Nevertheless, if we succeed, we can finally understand why
something hardly exists, namely female sexually selected weapons.
Acknowledgements I thank Bruce Lyon for fruitful discussions on this topic and for good comments on the manuscript.
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Current Zoology
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