Neuroscience and Biobehavioral Reviews 46 (2014) 519–533
Contents lists available at ScienceDirect
Neuroscience and Biobehavioral Reviews
journal homepage: www.elsevier.com/locate/neubiorev
Review
The trap of sex in social insects: From the female to the male
perspective
Laura Beani a,∗ , Francesco Dessì-Fulgheri a , Federico Cappa a , Amy Toth b
a
b
Department of Biology, University of Florence, Florence, Italy
Departments of Ecology, Evolution & Organismal Biology and Entomology, Iowa State University, USA
a r t i c l e
i n f o
Article history:
Received 10 February 2014
Received in revised form
14 September 2014
Accepted 22 September 2014
Available online 2 October 2014
Keywords:
Sexual selection
Male social Hymenoptera
Sexual behavior
Male neuroendocrine system
Polistes dominula
a b s t r a c t
The phenotype of male Hymenoptera and the peculiar role of males has been neglected and greatly
understudied, given the spectacular cooperative behavior of female social insects. In social insects there
has been considerable progress in understanding the molecular mechanisms behind haplodiploid sex
determination but, beyond that, very little is known concerning the neural, endocrine, and genetic correlates of sexual selection in males. An opportunity is being missed: the male phenotype in Hymenoptera
is a natural experiment to compare the drives of natural versus sexual selection. In contrast to females,
males do not work, they usually display far from the nest to gain mates, compete among rivals in nuptial
flights or for a symbolic territory at leks, and engage in direct or ritualized conflicts. By comparing the
available data on male paper wasps with studies on other social Hymenoptera, we summarize what we
currently know about the physical, hormonal, neural and behavioral traits in a model system appropriate
to examine current paradigms on sexual selection. Here we review male behavior in social Hymenoptera
beyond sex stereotypes: the subtle role of “drones” in the colony, the lack of armaments and ornaments,
the explosive mating crowds, the “endurance” race, the cognitive bases of the “choosy” male and his
immune defense. Social insect males are not just simple-minded mating machines, they are shaped,
constrained and perhaps trapped by sexual selection.
© 2014 Elsevier Ltd. All rights reserved.
Contents
1.
2.
3.
4.
5.
6.
Are insects a good model to explore sex-dimorphism in behavior and brain? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
The neglected drone: male social hymenopterans in the Darwinian scenario . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Mating syndromes of social Hymenoptera . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Male insects in neuro-endocrine research . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.1.
Organizational and activational effects of hormones on sexual behavior . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.2.
Male hymenopterans: a brain for just one season . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
A new model for cognitive and neuroendocrine adaptations under sexual selection: a focus on Polistes dominula males . . . . . . . . . . . . . . . . . . . . . . .
5.1.
The reproductive apparatus and immune defense, from a male perspective . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.2.
Studying lekking behavior: not just “child’s play” . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.3.
The smart male: from the field to the lab . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Wider challenges . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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1. Are insects a good model to explore sex-dimorphism in
behavior and brain?
∗ Corresponding author. Tel.: +39 055 22 881; fax: +39 055 222 565.
E-mail address: laura.beani@unifi.it (L. Beani).
http://dx.doi.org/10.1016/j.neubiorev.2014.09.014
0149-7634/© 2014 Elsevier Ltd. All rights reserved.
The evolutionary tree is not a hierarchy. It is tempting for all of
us to view animals with which we share a more recent common
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L. Beani et al. / Neuroscience and Biobehavioral Reviews 46 (2014) 519–533
ancestor as being just like us. Baboons and even bluebirds can
look and act an awful lot like people. A good deal of my own
research is done with insects, and one of the reasons I like working with them rather then with vertebrates is that is harder to
see myself reflected in their behavior.
Marlene Zuk, Sexual Selections. What We Can and Can’t Learn
about Sex from Animals, 2002, Introduction, p. 3.
The challenge of this review it is to describe what is known about
the forces of sexual selection which have shaped mating behavior, morphology and neuro-endocrine system of males in social
Hymenoptera: wasps, bees, ants; and also to provide a roadmap
for future studies by highlighting key questions for future research.
The male phenotype is like the dark side of the moon. However
it represents a natural experiment that has been greatly undervalued, to compare the drives of natural versus sexual selection,
parental versus mating efforts, and their associated neurogenomic
mechanisms. In social Hymenoptera males and females represent
two divergent morphs. The primary abode of females (queens and
workers) is the colony, whereas mating – the focus and the final
chapter of male life history – occurs mainly outside the nest. The
male, devoid of the constraints imposed by caste specialization,
may be viewed as the output of sexual selection.
In The Descent of man, and Selection in relation to Sex (Darwin,
1871), the actors of sexual selection are “ardent males and choosy
females”, i.e. male–male fighting and female choice. The “wonderful horns” of male rhinoceros beetles fit into Darwin’s armaments
category. Other traits, both morphological and behavioral, evolved
because the females preferred them, i.e. are ornaments: again, in
certain Coleoptera, “the splendid metallic tints” and “stridulating
organs” of males (Chapter XI, p. 422).
While competition among males for the rights to mate with a
female seemed reasonable enough to Darwin’s Victorian contemporaries, virtually none of them could swallow the idea
that females–of any species, but especially the so-called dumb
animals –could possibly do anything so complex as discriminating between males with slightly different plumage colors. [. . .]
Largely because of the opposition to the idea of female choice,
sexual selection as a theory lay dormant for several decades.
Marlene Zuk, Sexual Selections. What We Can and Can’t Learn
about Sex from Animals, 2002; Introduction, p.7.
Modern behavioral ecology has moved beyond the paralyzing
view of “dumb animals”, with an increasing appreciation for the
behavioral complexity and cognitive capacities of insects. Thus, in
addition to an easier evasion of the risk of anthropomorphism, studies on insects have played a lead role in developing new insights in
sexual selection (Table 1).
The brain is one of the most important sexual organs;
indeed, most sexual selection mechanisms rely on sensory/neural/cognitive differences among potential partners or
rivals. Neural plasticity and learning may be involved in mating
tactics, from competition to mate choice, from advertisement
displays to mate guarding and pair bonding, in birds (Keagy et al.,
2012) as well as in insects (Dukas, 2006, 2008) and other taxa. Neural sex dimorphism – in human and non-human animals – is the
obvious consequence of Darwin’s assumption: “sexual selection
has apparently acted on both the male and the female side, causing
the two sexes of man to differ in body and mind” (Chapter XXI,
p. 402). Brain sex differences involve developmental, ecological
and taxonomic differences. “Not all sexually selected traits are
conspicuous. However, and when a sex difference consists of an
enhancement of cognitive and perceptual ability, disentangling
the separate actions of natural and sexual selection is difficult”
(Jacobs, 1996). Nevertheless, some of these differences might be
best understood within the framework of sexual selection and, in
particular, in social Hymenoptera.
While female castes are hot topics in neuroscience and genetic
analysis, social hymenopteran males are seldom subjects of molecular and neural studies of behavior, being instead used to study
sex determination, sperm competition, long-term sperm storage,
with some exploratory studies on brain transcriptome expression
(mostly in Apis: Collins et al., 2006; den Boer et al., 2009; Stürup
et al., 2013; Zareie et al., 2013; Zayed et al., 2012). Excellent reviews
on genetic and genomic analyses in insect societies do not consider the male role, as this is surely marginal in terms of colony
division of labor (Smith et al., 2008). In contrast to males’ lack
of social behavior, the mating biology of male social hymenopterans involves cognitive abilities, is flexible and open to alternative
tactics. Thus, hymenopteran traits have been the result of diverse
selective forces – individual selection, kin selection, group selection, and sexual selection – acting across species and between males
and females.
The main goals of this review are: (i) to identify the role of males
in social Hymenoptera, in which a massive emergence of males
turns into collective mating syndromes; (ii) to organize the scarce
and scattered neuro-endocrine data on males in an updated theoretical scenario; and (iii) to provide an overview of behavior and
physiology of male Polistes dominula, a suitable model organism to
investigate the expression of sexually selected traits by means of
modern neuro-endocrine and genomic approaches.
2. The neglected drone: male social hymenopterans in the
Darwinian scenario
Eusociality, evolved in ants, bees, wasps and a few other taxa, is a
rare form of complex social behavior characterized by cooperative
brood care, reproductive castes (queens/kings and workers), and
overlapping generations (Michener, 1969). In the Hymenoptera,
these impressive feats of cooperation are entirely limited to the
female sex. Social insects are descended from solitary-nesting
ancestors where only females care for young (Davies and Gardner,
2014). Thus, in social as well in solitary species, females are involved
in nesting and brood care, due to sex-specific expression of genes
for parental behavior (West-Eberhard, 2003). Sexuals (males and
gynes, i.e. virgin potential future queens) typically emerge at the
peak of colony development (with some exceptions, Strassmann,
1981). Long-lived queens leave the colony and, after mating, will
start a new colony, whereas males die after the nuptial season (but
see Shik et al., 2013; Kureck et al., 2013 about longevity in male
ants).
Males lack the anatomical and behavioral adaptations to be efficient workers, such as the sting (Starr, 1985) and hunting and
foraging for brood provisions (West-Eberhard, 1975), with some
exceptions (see the moderately developed pollen baskets in bumble
bee males observed also by Darwin, a case of “cross-sexual transfer”, West-Eberhard, 2003). Not surprisingly, the sex ratio of the
colony is usually female-biased, a fact that has been recognized as
far back as Charles Butler’s 1609, The Feminine Monarchie, or the Historie of Bees, the first English book about beekeeping. In a bee hive,
the males are less than 5% of the total number of females (Wilson,
2007). As a rule, in colonies of eusocial insects, the investment in
males is one third of that in future queens (Trivers and Hare, 1976).
This asymmetry is the output of the reproductive conflict between
the queen and the workers, which are more related to sisters than
to brothers or sons due to haplodiploidy (Hamilton, 1972).
Sex is determined by multi-allelic sex-determining loci (SDL)
which, depending on the species, can consist of a single locus
(such as the gene complementary sex determination) or many loci
(Beukeboom et al., 2007). Females arise from fertilized diploid eggs
that are heterozygous at the SDL and males from unfertilized haploid eggs. Diploid males – homozygous at the SDL – are rare and
L. Beani et al. / Neuroscience and Biobehavioral Reviews 46 (2014) 519–533
521
Table 1
Recent studies on sexual selection mechanisms in insects.
Book/review/study
Sexual selection mechanism
Animal model
Focus
Andersson (1994)
Lloyd (1981, 1997)
Lewis and Cratsley (2008)
Thornhill and Alcok (1983)
Beani (1996)
Beani and Turillazzi (1999)
Zuk et al. (1998)
Contreras-Garduño et al. (2008)
Endurance
rivalry
Comparative approach
Bumblebees, Fireflies
Mating success of males active during a prolonged breeding season
Endurance as a measure of male quality, bioluminescent and
pheromonal signals
Persistent lekking and swarming behavior, “Marathoner
hypothesis” and delayed mate choice
West-Eberhard (1979)
Nakano et al. (2010, 2013)
Ryan (1990, 1998), Ryan and
Cummings (2013)
Kumaran et al. (2013)
Bonduriansky (2001)
Parker (2006)
Gwynne (2008)
Gershman et al. (2013)
Stutt and Siva-Jothy (2001)
Parker (1970)
Parker and Pizzari (2010)
Waage (1986)
Fedorka et al. (2011)
Gray and Simmons (2013)
Worthington et al. (2013)
den Boer et al. (2010)
Birkhead (2000)
Arnquist and Nilsson (2000)
Torres-Vila (2013)
Eberhard (1985, 1996, 2010)
Social insects
Pathogens, parasites
and sexual signals
Sensory trap
Sensory exploitation
Field crickets
Call parameters may attract both females and parasites
Rubyspot damselfly
Comparative approach
The red wing spot decreases under immune challenges
Male traits are attractive resembling stimuli salient in other
context (food detection, predation)
Male courtship songs rendering females motionless as bat calls
Males traits exploit pre-existing sensory biases of females
Moths
Comparative approach
Male mate choice
Sexual conflict
Sperm competition
Female promiscuity
Genitalia divergent evolution,
cryptic female choice
Fruit flies
Insects
Comparative approach
Insects
Crickets
Bedbug
Damselflies
Plant related chemicals as male lures
Pre- and post-copulatory choice in relation to search cost and
female quality
An overview of sexual conflict over mating and fertilization
Sexual conflict over nuptial gifts, including seminal contribution
Food fight over free amino acids of spermatophylax
Sexual conflict and traumatic insemination
Sperm displacement of rivals, morphology of penis and bursa
copulatrix
Fruitflies
Field crickets
Seminal fluid proteins allocation, effects of perceived competition
Strategic ejaculates in relation to acoustic cues
Social insects
Comparative approach
Meta-analysis
Moths
Comparative approach
Seminal fluid mediates ejaculate competition
Promiscuity as an evolutionary history of sperm competition
Direct effects of multiple mating on female fitness
Variation among females in re-mating propensity
Male and female genital co-evolution, post-copulatory female
choice, sexually antagonistic co-evolution
their fitness is reduced (but see Cowan and Stahlhut, 2004; Liebert
et al., 2005; Cournault and Aron, 2009). Interestingly, haploidy
appears to impose constraints on males, because in many species
they have “reinvented diploidy” by doubling nuclear DNA content
mainly in thoracic flight muscles and forelegs. This may serve to
boost expression of genes necessary to meet the energetic demands
of flight and may be driven by sexual selection, as the need to fly in
search of females is probably more critical to fitness than predator
avoidance and long distance dispersal (Aron et al., 2005).
What is the male role in the colony? In social bees, wasps or
ants, workers and soldiers are females. Males seem to represent no
more than a cost to the colony, “intra-colony parasites”, “examples
of absolute egocentrism” (Wilson, 1971). In the English Thesaurus,
“drone” is translated as “idler, scrounger, parasite”, although “a
more appropriate view is that of a frenetic male in desperate search
of an elusive, receptive female” (Paxton, 2005). As expected, male
altruism is rare (Table 2), independently of ploidy (for the evolution
of helping due to ecological factors and sex-ratio, see Ross et al.,
2013; Gardner and Ross, 2013). Overall, males of Hymenoptera
have no or only minor tasks in the colony (Hölldobler and Wilson,
1990); there are scattered records of larval feeding in polistine
wasps (Hunt and Noonan, 1979; Cameron, 1986; O’Donnell, 1999;
Sen and Gadakar, 2006; Sinzato et al., 2009); nest construction and
defense in apoid wasps (Brockmann, 1992; Lucas and Field, 2011);
fanning on the nest to control brood temperature in bumble bees
(Cameron, 1985); trophallaxis by males of Camponotus ants living
for a long time in their nest (Hölldobler, 1966); silk production by
male larvae in the weaver ants (Wilson and Hölldobler, 1980). Thus,
in social Hymenoptera, males are typically of the “drone” type, while
the “helper” type is well represented in termites (where males are
diploid, and workers and soldiers are often immature and with little
sex-dimorphism, see Noirot, 1989, 1990; Thorne, 1997), and male
helpers appear also in other non-hymenopteran eusocial taxa (Choe
and Crespi, 1997).
Because male hymenopterans are lacking conspicuous armaments and ornaments (see Baer, 2014), it is not surprising that
Darwin, in The Descent of Man, and Selection in Relation to Sex,
devoted just two pages to Hymenoptera out of two chapters
reserved to insects. Overall, male fighting appears to be an ancestral trait (Heinze et al., 2005) that was subsequently lost and now
uncommon in these taxa. Fighting is often associated with a strong
investment in size in males. Darwin noted that male social insects
may be “pugnacious”, but in only a few cases they are “larger and
stronger than the females. On the contrary, they are usually smaller,
so that they may be developed within a shorter time, to be ready in
Table 2
Male ‘types’ in social insects (H = haploid male; I = inbreeding; O = outbreeding).
’Drone’ type
’Helper’ type
Hymenoptera: bees, wasps,
ants (H,O) [Bartz (1982)]
Homoptera (Pemphigidae,
Hormaphididae): aphids
with female sterile soldiers
for housekeeping in galls and
winged dispersing males (O)
[Benton and Foster (1992),
Stern and Foster (1997)]
Coleoptera: Austroplatypus
incompertus, an ambrosia
beetle with female subfertile
helpers and males leaving
the gallery-nest (O) [Kent
and Simpson (1992), Kent
(2002)]
Isoptera: soldiers and workers of both
sexes (I/O) [Muller and Korb (2008)]
Thysanoptera: gall-induced thrips,
micropterous soldiers of both sexes,
male guarding on egg mass (H,O)
[Crespi (1992), Choe and Crespi (1997),
Chapman et al. (2000, 2002)]
Coleoptera (Platypodidae e Scolytidae):
ambrosia and bark beetles with male
helpers at the nest (I) [Kirkendall
(1993), Kirkendall et al. (1997),
Biedermann and Taborsky (2011)]
From Beani and Turillazzi (2002). References have been updated.
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large numbers for the emergence of the females” (p. 264). According
to Darwin, sexual size dimorphism is the rule throughout solitary
and social Hymenoptera (Stubblefield and Seger, 1994). Body size
of males is rarely smaller than workers but usually smaller than that
of queens (Boomsma et al., 2005). Aggressiveness among rivals, as
well as a high mating frequency, are more common in relatively
large males of social wasps and bumble bees, while small male ants
form mass swarms and the proportion of male multiple mating is
lower.
But do ornaments matter for male social insects more than
armaments? “The power to charm the female has been in some
instances more important than the power to conquer other males
in battle” (Darwin, 1871, Chapter VIII, p. 279). The only male ornaments so far described in social insects are the elliptical yellow
abdominal spots in the paper wasp Polistes dominula (Izzo and
Tibbetts, 2012), the black pigmentation on the head of P. simillimus
(de Souza et al., 2014) and the sexually dimorphic white stripes
displayed by male stenogastrine wasps by fully stretching their
abdomens during their costly hovering and aerial duels (Beani and
Turillazzi, 1999). Overall, Darwin (1871) rightly underlines that in
Hymenoptera males are “inconspicuous, being defenceless. Slight
differences in color, according to sex, are common, but conspicuous differences are rare except in the family of Bees (. . .), especially
in the solitary species” (p. 237), which do exhibit some sex dimorphism (see also Stubblefield and Seger, 1994).
3. Mating syndromes of social Hymenoptera
Social hymenopterans differ from solitary species for “the production for this single purpose of thousands of drones, which are
utterly useless to the community for any other end, and which
are ultimately slaughtered by their industrious and sterile sisters”
(Darwin, 1859, Chapter VI, p. 202). But male hymenopterans are
not “useless” at all in terms of colony fitness. Their ultimate goal is
undoubtedly mating: they are driven by the “developmental trap
due to sexual selection”, a bottleneck which screens for indicators of good genes in males and subtle discrimination for sexual
signals in females (West-Eberhard, 2005). “Vigorous, and in other
respects the most attractive males” – to reuse the words of Darwin
(1871, Chapter VIII, 262) – are not directly represented in “sexy
sons”, because males do not sire sons but only female offspring due
to haplodiploidy. But a long-term paternal effect of mate choice
is likely to act on “sexy grandsons” and on the fitness of all the
colony members. Sexual selection has a profound effect on the evolution of complex societies (Rubenstein, 2012), because offspring
relatedness is ultimately determined by mating systems. Monandry
is the ancestral and more frequent state of social Hymenoptera
(Boomsma and Ratnieks, 1996; Strassmann, 2001), but it is interesting to note that extreme polyandry has evolved as a derived trait
in a few highly social lineages (honey bees, leafcutter, army and
harvester ants, and vespine wasps (Hughes et al., 2008; Boomsma,
2009). If single paternity is widespread, the role of sexual selection
is critical to determine the most competitive or most preferred male
by females (Baer, 2014).
Relatively few studies (see Alcock et al., 1978, the first comparative paper on this topic) are devoted to the evolution of male
mating strategies in Hymenoptera for at least three good reasons (Boomsma et al., 2009). First, exclusion is attributable to
the “spectacular” emphasis on the Hamiltonian predictions about
relatedness and eusociality. Second, it can also be explained by
the fact that “male ornaments and sperm displacement devices are
absent and male fighting rare”. Third, practical considerations may
be at fault, because hymenopteran mating behavior is “very hard
to study in the field (and close to impossible in the laboratory)”
(Boomsma et al., 2009). In fact, the two major mating syndromes,
female calling and male aggregation, first proposed by Hölldobler
and Bartz (1985) and then extended to social wasps and bees
(Ayasse et al., 2001), are ephemeral pre-copulatory phenomena
that are difficult to observe and study. Because social insect males
are “elusive” (Shik et al., 2013), the knowledge gap about their
behavior and physiology is not surprising (but see the special issue
of Apidologie devoted to “the neglected gender: males in bees”,
Koeniger, 2005; Hrassnigg and Crailsheim, 2005).
The nuptial systems of social insects, unlike solitary species,
have been classified as scramble competition at explosive mating assemblages and prolonged lek polygyny, due to their massive
production, low mate monopolization potential and widespread
outbreeding (Thornhill and Alcock, 1983; Alcock and Thornhill,
2014). Sex pheromones, released by both sexes, induce impressive
aerial or substrate-based swarms (Sivinski and Petersson, 1997;
Shelley and Whittier, 1997), spatially organized around speciesspecific landmarks or hilltops, receptive females, more rarely,
within or close to natal nests (see lethal fights for a harem of
queens among wingless males of Cardiocondyla ants, Heinze and
Hölldobler, 1993).
With regard to post-copulatory mechanisms, both sexes may
influence the strategic allocation of ejaculates. Males of honey bees,
stingless bees and army ants mate singly whereas multiple mating
by males is common in bumble bees and social wasps (Boomsma
et al., 2005). After eclosion, males produce a fixed amount of clonal
sperm; nonetheless, sperm gene expression shows substantial variation that may affect sperm morphology and fertilization ability
(Higginson and Pitnick, 2011). Due to the limited amount of spermstorage, we can expect male mate choice and some effect of seminal
fluid on sperm viability. But males of social Hymenoptera have “no
influence on the fate of ejaculates after mating” (den Boer et al.,
2010): they just survive as stored sperm
Males have been regarded as “simple and small mating
machines” or “flying sperm containers” (Tsuji, 1996; Baer, 2003).
Although they do not display spectacular sexually selected traits,
males are not simple-minded organisms. While not strictly social,
they can be highly gregarious in their collective nuptial parades,
where they may perform impressive sexual displays. They are also
capable of behavioral flexibility in the form of alternative mating
tactics, possess sophisticated chemical – and perhaps visual – perception to find females, and in some cases exercise subtle mate
choice. In his concluding remarks on insects, Darwin (1871) points
out that the sexes “differ in their sense and means of locomotion,
so that the males may quickly discover and reach the females”, as
well as in devices “for retaining the females when found” (p. 264).
Sexual selection, according to the drone role outside the colony,
should act on sensory and physical skills to gain fast but lasting
access to females, rather than on male attractiveness and fighting
abilities. In a general sense, their life history is similar to that of
workers: they spend the first days inside the nest and venture outside for orientation, lekking and mating flights (Stürup et al., 2013).
Males are targets of both pre- and post-copulatory pressures and
are thus excellent models to study the action of sexual selection,
from a behavioral as well as from a neuro-endocrine perspective.
4. Male insects in neuro-endocrine research
4.1. Organizational and activational effects of hormones on
sexual behavior
Unlike vertebrates, where sexually selected traits are mostly
controlled by androgens and estrogens produced by gonads
and extra-gonadal tissues, insect sexual development has been
regarded as strictly genetic, dependent on “cell-autonomous
expression of sex specific genes”, independent of the hormonal
milieu (Bear and Monteiro, 2013). Each cell is thought “to know its
L. Beani et al. / Neuroscience and Biobehavioral Reviews 46 (2014) 519–533
sexual identity” according to information on the sex chromosomes
(Robinett et al., 2010). However, in the last decade, a comparative approach using both invertebrates and vertebrates suggests
the existence of counterparts in insects for reproductive hormones
and neuropeptides (De Loof, 2008; Van Wielendaele et al., 2013).
As in vertebrates, the concepts of organizational and activational hormonal effects apply to insects, allowing for a continuum
between variation in early hormone levels, neural substrates and
behavior (Elekonich and Robinson, 2000). In insects the hormones that control molting and growth can partly or totally
affect sexually selected traits, and thus act as sex hormones: the
lipophilic ecdysteroids (E), the precursor of the molting hormone
20-hydroxyecdysone (20E), produced in the prothoracic gland,
ovaries, oenocytes and other tissues, and juvenile hormone (JH),
produced in the corpora allata, a distinct pair of glands in the retrocerebral complex, and probably in accessory glands (De Loof et al.,
2013). In these taxa, the masculinizing or feminizing action of hormones depends on the sex of the subject, its stage of development,
the timing and the target tissue.
The role of ecdysteroids as sex hormones and developmental
factors in insects is probably underestimated (De Loof, 2006). Not
surprisingly, ecdysteroids and JH play a role in male sexual maturation and the activity of the accessory gland (Happ, 1992; Gillot,
1996), a structure under strong sexual selection because its secretions, transferred to the female, are essential for mating success in
terms of female physiological and behavioral manipulation, sperm
survival and sperm competition (den Boer et al., 2013). Genes for
the synthesis of ecdysone (E) are expressed in the accessory glands
of beetles and fruit flies, while the gene encoding the enzyme mediating 20E synthesis was detected in the ovaries of females (Hentze
et al., 2013). It is likely that “E and 20E have sex-specific roles analogous to the vertebrate sex steroids, where males produce primarily
testosterone, the precursor of estradiol” (Hentze et al., 2013). However, an effect on male reproductive behavior of ecdysteroids has
not been clearly demonstrated.
On the other hand JH, the “status quo” factor in molting and
metamorphosis and “a master regulator of the female reproduction
syndrome” (Hartfelder, 2000), plays a multifaceted role in controlling many aspects of sexual behavior: dispersal and nuptial flights,
calling behavior, courtship, post-copulatory changes in the female,
and oviposition. “Quite different from the more conserved role of JH
as a modulator of ecdysteroid action in larval-pupal development,
the roles of JH in adult insects are, at a first sight, rather confusing.”
(Hartfelder, 2000).
Evidence of hormonal effects on male sexual behavior in insects
is somewhat scattered. As regards armaments and ornaments, JH and
ecdysteroid titers influence horn growth during the development of
the dung beetle Onthophagus taurus, resulting in males with long
horns, rudimentary horns or no horns at all (Emlen and Nijhout,
1999). In male cockroach fights, JH levels affect both rank establishment (Kou et al., 2009) and sex pheromone production (Sréng et al.,
1999), i.e. both male-male competition and female choice, because
“odor conveys status” (Moore et al., 1997). In the noctuid moth
Agrotis ipsilon, JH increases the neural sensitivity of male antennal
lobes to female sex pheromones (Duportets et al., 2013). Many of
the effects induced by JH hormones are costly (Teal et al., 2013):
in the tephritid flies Anastrepha and Bactrocera, the administration
of methoprene (JH-analog) increases male sex pheromone production, lekking behavior, courtship, and mating success when males
are supplemented with proteins (but see Shelly et al., 2009). From
this perspective it not surprising that JH action (or JH directly) may
have an immunosuppressive effect (Rantala et al., 2003), in agreement with the immunocompetence handicap hypothesis (Folstad
and Karter, 1992; see Schmid-Hempel, 2011).
In honey bees, the sexual maturation of drones, which terminates with nuptial flights, is modulated by the endocrine system:
523
the JH titer gradually rises during adulthood (Giray and Robinson,
1996) due to increased synthesis in the corpora allata (Tozetto et al.,
1995), while the ecdysteroid titer decreases. Experimental manipulations of ecdysteroids have shown they are potent modulators of
protein synthesis in the mucus glands during larval sexual maturation (Colonello and Hartfelder, 2003). On the other hand, JH does
not affect maturation of reproductive organs such as testes, seminal vesicles, and mucus glands but regulates in-hive behaviors such
as movements and diet transition (Harano, 2013) and the onset of
mating flights (Giray and Robinson, 1996; Tozetto et al., 1997).
Many of the effects of JH on male behavior are mediated by
dopamine (DA). Harano et al. (2008) showed that DA system is
downstream of JH by applying a JH analog onto drones. Akasaka
et al. (2010) and Mezawa et al. (2013) showed that DA influenced
flight activities. JH-elicited DA signals may influence flight initiation in honey bee drones as well as in carpenter bee males (Sasaki
and Nagao, 2013). The regulation of reproductive behaviors by JHDA signaling in drones resembles that of more primitively eusocial
insects such as female bumble bees and paper wasps (Sasaki et al.,
2012), while in female honey bees ovarian development is DAregulated (reviewed by Sasaki and Harano, 2010) and JH is the
major determinant of caste differentiation and worker-specific foraging (Robinson, 1987). A possible linkage between JH and DA
might be conserved in honey bee males but lost in their females
in the course of social evolution (Sasaki and Harano, 2010; Sasaki,
2013).
4.2. Male hymenopterans: a brain for just one season
“Perhaps these insects are little machines in a deep sleep, but
looking at their rigidly armored bodies, their staring eyes, and
their mute performances, one cannot help at times wondering
if there is anyone inside.”
Vincent G. Dethier, To Know a Fly, 1962
The contributions of the entomologist and physiologist Vincent
Dethier, in establishing a continuum between the “microscopic
brains” (1964) of insects and the larger brains of vertebrates, was
aptly highlighted by Marlene Zuk in the chapter of Sex on Six Legs
devoted to The Inner Lives of Wasps (2011). Among hymenopterans, brain research has first focused on Apis mellifera (Kenyon,
1896), because brain dissection is easier in larger insects, and caste
differentiation and communication provide great opportunities to
evaluate neural plasticity and divergent pathways. Overall, insect
brains are composed of sensory, motor and multimodal central
components. The mushroom bodies bear a striking resemblance
to the mammalian cortex due to their modular organization in cell
subpopulations (Farris, 2005), the fact that they combine visual and
olfactory inputs, and their involvement in learning, memory, initiation of motor activity, decision-making processes (Strausfeld et al.,
1998) and sleep (Joiner et al., 2006). The central complex plays a role
in organizing behavior, because it integrates sensory inputs (polarized light information) and motor commands (Strausfeld, 1999;
Strauss, 2002).
With regard to vision, hymenopterans are generally equipped
with three (bees and wasps) or two (ants) photo-pigments for
UV and color vision (Briscoe and Chittka, 2001), and are able to
process information about motion, patterns, direction and landmarks (Strausfeld, 1989). Large eyes and large optic lobes (lamina,
medulla, lobula), the primary vision centers, suggest complex visual
processing. Antennal sensilla, with thousands of olfactory receptor
neurons terminating in the glomeruli of the antennal lobe are the
primary olfactory centers, and perceive mechanical stimuli, humidity, temperature, carbon dioxide concentration and an infinite
number of chemical cues: “ordinary” odors, but also pheromones
(see Korsching, 2001 for a review in insects and vertebrates).
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L. Beani et al. / Neuroscience and Biobehavioral Reviews 46 (2014) 519–533
Fig. 2. Scanning electron micrograph of the head of a gynandomorphic honey bee.
Right antenna and compound eye worker-like, left antenna and compound eye
drone-like.
From Brockmann and Brückner (1999).
Fig. 1. The relatively large brain of a female Polistes dominula (top) and the “miniaturized” brain of a worker ponerine ant Pachycondyla villosa (bottom). Microtome
section (15 ␮m) of osmium-stained material. Labels: antennal lobe (al), mushroom
body caliyx (ca) and lobes (mbl), central body (cb), lamina (la), medulla (me), lobula
(lo), protocerebral lobe (pc), median ocellus (oc).
From Gronenberg et al. (2007).
Very few studies have examined the brain of paper wasps
(Ehmer and Hoy, 2000; Ehmer et al., 2001; O’Donnell et al., 2013,
2014). Brain structure (Fig. 1, Gronenberg et al., 2007) has been
recently analyzed in Polistes species where females seem to use
facial cues to discriminate conspecifics (Tibbetts, 2002; Tibbetts
and Dale, 2004; Sheehan and Tibbetts, 2011; but see Cervo et al.,
2008). This ability is related to subtle changes in the size of the
mushroom bodies and antennal lobes. Again, females, not males
have been the focus of studies on functional neuroanatomy, brain
allometry and neuroplasticity (Gronenberg and Riveros, 2009).
Unlike in bees and wasps, in ants there has been “a major emphasis on olfactory and pheromone processing and relatively less
prominence of visual processing” (Gronenberg, 2008). This ability is strictly related to social tasks and communication inside the
“female superorganism”, because in insects, unlike in vertebrates,
there are no specific “social” brain components.
But what about the male brain? Studies devoted to sexual
dimorphism in the chemosensory system and the brain structure
of social hymenopterans are very scarce, despite the fact that male
sexual performance is costly and surely involves specialized motor
and cognitive skills (Table 3).
A common approach has been to assay neural development and
changes by comparing males and workers. Overall, the number
of glomeruli reflects the richness of antennal olfactory receptors,
this input is then processed in the MBs and in the protocerebrum, together with other sensory information. Males usually have
fewer glomeruli than females but do possess four macroglomerular complexes, i.e. sex-specific hypertrophied glomeruli (see for
a definition, Streinzer et al., 2013b). This striking difference may
reflect the multiplication of sex-pheromone-sensitive sensory neurons. Male eyes and/or antennae are enlarged because they are
selectively tuned to detect receptive females or pheromones. In
gynandromorphic honey bees, depending on the mosaic pattern
of the head, one antenna – and its antennal lobe – can be dronelike and the other worker-like (Brockmann and Brückner, 1999,
Fig. 2). In contrast to the increase in eye and antenna size, males
have reduced communication within the colony as well as a simpler
behavioral repertoire. In line with this, MBs are smaller in males
compared to females in Hymenoptera compared to other insects
(Streinzer et al., 2013b).
Notably, the only study on paper wasp males (Molina
and O’Donnell, 2008, see Table 3) is focused on “unusual”
males with female-like behavior (O’Donnell, 1999). Mischocyttarus mastigophorus males remain on their natal nests and
show dominance behavior toward females, taking food from
incoming foragers. Like females, more aggressive males have an
enlarged antenna-innervated MB component, suggesting these
males receive olfactory and tactile information useful for nestmate recognition. Individual males who frequently leave the nest
for mating opportunities (in this genus along patrol routes or at
nuptial arenas see Litte, 1979, 1981) have larger MB than females
in the calyx region, which receive optic information. Searching for
females requires enhanced peripheral and central visual processing
and flexible cognitive strategies. Age is a positive predictor of MB
calyx volume in both sexes.
The brains of honey bee drones have been better explored:
the striking dimorphism between workers and drones is probably enhanced by their different lifestyles (Fig. 3). Drones are
Fig. 3. Sexual dimorphism of the peripheral olfactory system and its representation
in higher brain centers in Apis mellifera drone and worker. Labels: antennal lobe (AL),
mushroom body (MB), central body (CB), lobula (Lo), remainder of supraesophageal
ganglion (SEG).
Modified from Streinzer et al. (2013b).
L. Beani et al. / Neuroscience and Biobehavioral Reviews 46 (2014) 519–533
525
Table 3
Sex differences in sensory and brain development of social hymenopterans. OL = optical lobes, AL = antennal lobes, MB = mushroom bodies, CB = central bodies, HC = cuticular
hydrocarbons.
Study
Animal model
Sensory centers
Brain specialization
Focus
van Praagh et al. (1980)
Arnold et al. (1985)
Menzel et al. (1991)
Brockmann et al. (1998)
Nishino et al. (2009)
Streinzer et al. (2013a,b)
Alford (1975)
Alcock and Alcock (1983)
Ågren and Hallberg (1996)
Streinzer and Spaethe (2014)
Honeybee drones, respect
to workers, have:
Extended acute zone in the
dorsal eye region
Elongated antenna and
flagellum, more sensilla
placodea,
Larger optic lobula
AL with a less glomeruli and
macroglomeruli
Smaller MB
Bumblebee drones
(Bombus spp.), which may
scent-mark patrol routes or
wait for females at perches
have:
Larger eyes, higher number
of ommatiia in case of
waiting at perches
Elongated antenna
Flagellar sensilla on
antennae
Ocelli, larger compound
eyes with 1000–1500
ommatidia
Sex-specific acuity related to
mating behavior
Selective detection of
sex-pheromone
Low investment in learning and
memory
No conspicuous species-specific or
behavior-related differences for
flagella types and density
Larger OL (medulla and lobula)
AL with a less glomeruli and
macroglomeruli
Smaller MB
Larger CB
Similar volume of OL and AL
Larger MB calyx collars
Smaller MB calyx lips
Acute vision, less plasticity,
“hard-wired” behavior
Gronenberg (2008)
Mysore et al. (2009)
Nakanishi et al. (2009, 2010)
Ant males (Camponotus
spp. and other) respect to
workers, have:
Molina and O’Donnell (2008)
Males of paper wasp
Myschocyttarus
mastigophorus, respect to
females, have:
“embedded in the protective social network and leave the colony
only for short, synchronized mating flights” (Streinzer et al., 2013b)
to congregate at landmarks, waiting for a queen (guided by olfactory and visual cues, Winston, 1991). If unsuccessful, they can
return to their colonies, so forays outside the nest are short and
males are unable to forage and feed themselves (Ruttner, 1966;
Koeniger et al., 2005).
Further research linking male sexual behavior and neural organization is surely needed to understand how experience can modify
brain development in many subtle ways (Jones et al., 2013).
Changes in brain size and organization might reduce the “global
cost” of neural tissue in the evolution of learning and memory
(Snell-Rood et al., 2009). In male song birds, the neural system
involved in song control changes in relation to courtship and vocal
performance: “a brain for all seasons” (Nottebohm, 1981). Although
the nuptial season is brief for insect males, neural plasticity may
play a key role if alternative nuptial strategies occur. Behavior and
brain development, including MB reorganization, are influenced by
juvenile hormone (JH) titers in worker honey bees, which change
as they switch tasks with age (Fahrbach and Robinson, 1996). Males
could provide an excellent reference point, independent of sociality, to investigate the influence of sexual selection on both neural
development and gene expression (Zayed et al., 2012). Males of
solitary and some social hymenopterans, like bumble bees or paper
wasps, abandon the nest and have to survive for days or weeks outside; thus, we would expect a lower degree of sex-dimorphism or
other adaptations, such as sex-specific odor detection and locomotion/defensive abilities, when compared to the less self-supporting
honey bee drones.
5. A new model for cognitive and neuroendocrine
adaptations under sexual selection: a focus on Polistes
dominula males
In the primitively eusocial paper wasp Polistes, a model
organism in evolutionary biology (Starks and Turillazzi, 2006),
morphological castes are not clearly differentiated, but genetic
relatedness is always fairly high (Strassmann et al., 1989). These
wasps are not only manageable as laboratory animals for experimental manipulation, but also suitable to explore the brain gene
expression underlying reproductive and brood provisioning status,
i.e. the evolution of castes (Toth et al., 2007, 2009, 2010). Studies of brain gene expression in P. metricus, indicate that there are
Greater visual capabilities
Lower chemosensory capacity
Gender- and age-related effects on
brain volume
some conserved genes and pathways associated with foraging and
aggressive behavior in both bees and wasps, suggesting that there
may be a “genetic toolkit” for certain forms of social behavior across
social taxa (Toth et al., 2010, 2014). It is of interest to note that
several genes associated with female dominance behavior in P.
metricus were also associated with male territorial aggression in
Drosophila (Edwards et al., 2006), suggesting that some genes retain
deeply conserved functions in aggressive behavior across a wide
variety of taxa and across sexes (Toth et al., 2014).
An overlooked key factor is the diversity of lifestyles among
males. Unlike honey bee drones, males of paper wasps lack colony
support. P. dominula males – variable in body size but slightly
smaller than gynes like other wasps – are barely tolerated (Starks
and Poe, 1997) and leave their colonies shortly after emergence
(at around one-two weeks of age). Like bumble bees, they have
to survive for days far from the nest, face pathogens and parasites, compete with rivals, and search for receptive females. In most
Hymenoptera, male lifespan is around two-three months, e.g. in
temperate species, from mid-July to October, and they do not overwinter. From an evolutionary perspective, “Live hard, die young”
is an apt description of Hymenoptera male reproductive strategies
(Zuk, 1990; Zuk and Stoehr, 2010).
Alexander et al. (1997) argued that, in insects, learning in the
context of courtship and mating is negligible due to their short
lifespan. Conversely, Reuven Dukas (2006) stressed that males
have many opportunities to learn (e.g. to avoid sexually deceptive
orchids, Ayasse et al., 2001), especially if they spend their lives
outside the colony like paper wasp males do. In theory a male
could embark on a mazy decision-making pathway of reproductive strategies (Edward & Chapman, 2011, Fig. 4), in which he may
choose tactical changes and sometimes mate rejection. In all of
these areas, P. dominula males are an ideal study system. Here, we
review a relevant body of behavioral and morpho-functional features of male P. dominula, from classical studies to recent results
(Table 4), and conclude that lekking males represent an ideal –
not yet exploited – system to study how sexual selection shapes
cognitive and perceptual skills.
5.1. The reproductive apparatus and immune defense, from a
male perspective
“The new bridge between sexual selection and reproductive
physiology”, advocated by Eberhard and Cordero some years ago
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Table 4
A list of potential sexually selected traits in Polistes dominula males.
Behavioral repertoire
Focus
Morpho-functional analysis
Focus
Study
Leks at traditional
landmarks, field and
lab study
Rubbing abdomen and
legs on the substrate
Landmark- based
system in 4 Polistes
species
Nuptial systems in
paper wasps,
comparative
approach
Sperm number in
relation to single
mated females
Antennal courtship
Large residents and small
transients
Body size overlap between
residents and transients
Condition dependent strategy,
flexible tactic
Beani and Turillazzi (1988)
Resident males mark peculiar
spots inside territories
Temporal and spatial
segregation
Sternal and leg tegumental
glands
Hypothesis of a pheromonal
release
Beani and Calloni (1991a,b)
Rare copulations late in the
season, endurance rivalry,
marathoner hypothesis
Antennal vibrations and grasps
are indicator of mating success
Unmated females were
attracted to male odor, but not
the reverse
Sexual trials in lab
between nestmates
Male competition and
female choice in lab
studies
Sexual preference trials
in lab
No clear avoidance of both
nestmates and inbreeding
Small elliptical abdominal
spots as quality signals
Bimodal-size sample,
lab study
Beani (1996)
Post-emergence maturation of
reproductive apparatus
Sex attraction by
olfactomer bioassays
Sexual selection in lab
by parasitized males
Beani et al. (1992)
Males avoid workers and
sexually interact with gynes,
healthy and parasitized
(castrated)
Parasitized males maintain
their sexual behavior and
preference
Territorial strategy, more than
size, affects mating success
Class 3 sex dimorphic glands in
antennae with ampulla-like
reservoires
Male glands in gaster and legs
One month old males store a
growing number of sperm
waiting for females
Hypothesis of a pheromonal
release
Salerno and Turillazzi (2001)
Orientation rather than
copulatory behavior:
interference from alarm
pheromone venom?
MacKenzie et al. (2008)
Romani et al. (2005)
Liebert et al. (2010)
Izzo and Tibbetts (2012)
HC profiles differ among
workers and gynes, no parasite
effect
Caste chemical cues orient
male choice, regardless of the
reproductive value of females
Cappa et al. (2013)
Histological analysis of male
apparatus
The parasite Xenos vesparum
does not heavily affect the
apparatus
Apparatus development
unrelated to body size, larger
AG are associated with more
copulations
The parasite Xenos vesparum
does not heavily affect the
apparatus neither the size of
CA
Honeybee male larvae have
higher susceptibility to
bacteria than wasp male larvae
Cappa et al. (2014)
Analysis of testes, seminal
vesicles and accessory glands
(AG)
Age and parasite effects
Structure/ultra-structure of
male reproductive apparatus,
corpora allata (CA)
Haplodiploid
susceptibility
hypothesis
Bacterial challenge to test the
immune response of males and
females
(1995) emphasizes the importance of avoiding a focus on each sex
separately. The male reproductive apparatus of Polistes (Fig. 6) was
surely an object of less attention than the ovaries, which serve as “a
kind of biography” (West-Eberhard, 1996) for female paper wasps,
despite the fact that sexual structures are deeply co-evolved.
Adult males emerge sexually immature, like females; when they
leave the colony, at around 2 weeks of age, they are able to copulate
(Beani, pers. obs.) and are equipped with a fixed amount of stored
sperm because testes degenerate 10 days after emergence (Salerno
and Turillazzi, 2001). The large discrepancy between the number
of sperm found in the vesicles of mature virgin males (≈500,000
in unmated 30-days old males, (Salerno and Turillazzi, 2001) and
in the spermatheca (≈6800 sperm), suggests that the male may be
polygynous and the female monandrous, as in most polistine wasps
(Strassmann, 2001, but see recent data on multiply paternity in
Polistes, Seppä et al., 2011, and in bumble bees, Owen and Whidden,
2013). Thus, the capacity to mate and intrasexual competition for a
receptive female is potentially high (Edward & Chapman, 2011, see
Fig. 4) and the male reproductive strategy is influenced by age and
sperm storage. Male multiple mating with the same or different
females has been often recorded in Polistes (Beani, 1996; Izzo and
Tibbetts, 2012; Beani and Zaccaroni, 2014) although it does not
Beani and Zaccaroni (2014)
Unpublish. data
Cappa et al. (in press)
necessarily imply multiple inseminations. This mismatch between
single paternity and repeated mating has been highlighted by Baer
(2014) in other monandrous social insects.
The general absence in wasps of genital plugs or peculiar
devices to displace sperm (Richards, 1978; Eberhard, 2004) could
be balanced by the evolution of “non-genital contact structures” (Eberhard, 2010) beyond the sclerotized clasping parameres
(Fig. 5), which are species-specific, as in other Hymenoptera
(Eberhard, 1996). For example, the curled antennae of P. dominula grip and rub female antennae during the brief period of mating
contact (West-Eberhard, 1969), and are covered by sensilla and
secretory glands, and may be a possible source of sex-pheromones;
thus antennation in males could be critical for social interactions, as in females (Romani et al., 2005). Inside a large cage we
observed both frequent antennal copulatory courtship, combined
with coupling and mate guarding (Beani and Zaccaroni, 2014). Postcopulatory female choice is likely happening in P. dominula. The
long spermathecal duct of female P. dominula, with a large reservoir and glands opening directly into the duct, as in other Polistinae
(Gotoh et al., 2008, 2009), might allow both sperm storage and
selective sperm utilization (Eberhard, 1996). Sperm expulsion by
females (Boomsma and Ratnieks, 1996) likely represents a form of
L. Beani et al. / Neuroscience and Biobehavioral Reviews 46 (2014) 519–533
Fig. 4. Selection for male mate choice is affected by mating and parental efforts,
operational sex ratio (OSR), potential reproductive rate (PPR), but also by the ratio
of available females/male mating capacity, a factor that is often undervalued, as well
as the variation in female quality.
From Edward and Chapman (2011).
cryptic choice by females. In P. dominula, we observed a female that
was grasped in flight by a male, the two wasps fell on the ground,
and this was accompanied by the ejection of a dense liquid drop
containing sperm (Beani and Zaccaroni, 2014).
The role of male accessory glands (AG), which grow with age
and are the source of a blend of secretions, would indeed be of special interest, due to the long sperm storage before reproduction.
These glands, which are widespread in insects (Gillot, 1996; Gillott,
2003; Simmons, 2001), can influence female reproductive physiology and behavior through secretory proteins and antimicrobial
peptides (Avila et al., 2011) transferred with sperm during copulation (Eberhard and Cordero, 1995). They are deeply involved in
“the chemical warfare between sexes”, as described by Baer (2003),
who stressed the necessity of a proteomic approch (Baer, 2014). In
a sample of males interacting inside a large cage, the size of AG
was significantly related to the number of copulations (Beani and
Zaccaroni, 2014). In line with our data, in D. melanogaster, males
with larger glands mated at a higher frequency than did males with
smaller glands, regardless of body size (Bangham et al., 2002). Body
size was not related to size of testes, vesicles, or AG; this development of AG, independent of the size, mirrors what is seen in
Polistes females, where large size is not an absolute predictor of
well-developed ovaries (Dapporto and Palagi, 2006).
Morpho-functional studies on the male reproductive apparatus of P. dominula are still needed. To date, a natural experiment
involving a parasite of these wasps suggests that neuro-endocrine
mechanisms may differ between sexes. The parasitic castrator
Xenos vesparum (Strepsiptera) produces dramatic phenotypic
alterations in their P. dominula hosts. Parasitized females have
527
undeveloped ovaries and desert the colony without performing any
social tasks (Hughes et al., 2004; Beani, 2006; Beani et al., 2011).
In a pioneering neuroendocrine study (Strambi et al., 1982), parasitized females were found to have smaller JH-secreting organs
(corpora allata) and lower JH-levels. In contrast, the volume of the
corpora allata in males decreases with age, as expected, regardless
of parasite’s presence (unpublished data). Moreover, neither the
structure of the male reproductive apparatus (Fig. 5) nor the sexual
performances were seriously compromised by the parasite (Cappa
et al., 2014, Fig. 6), although subtle differences might occur in AG
proteins of parasitized males (unpublished data).
Both pathogens and parasites may affect sexual traits (Zuk, 1990,
2009; Zuk and Wedell, 2014). The controversial but highly heuristic “sicker sex hypothesis” predicts that males will have a lower
immune defense compared to females (Poulin, 1996a,b). In social
hymenopterans, there is a combined influence of genetic (“haploid
susceptibility hypothesis”, O’Donnell and Beshers, 2004) and environmental factors (i.e. the investment in individual versus social
immunity, depending on male lifestyle). Given that the sex of the
host may have a strong influence on the impact of a parasite (Zuk
and McKean, 1996; Cappa et al., 2014), we compared bacterial
clearance in larvae of P. dominula and A. mellifera of both sexes
(Cappa et al., in press). In agreement with predictions based on
behavioral dimorphism, males of P. dominula, which spend a greater
proportion of their lives away from the nest, showed higher bacterial clearance than workers. Honey bee drones, which benefit from
the protection of the colony for most of their lives, had a higher
susceptibility to bacteria compared to workers (in agreement with
Laughton et al., 2011). However, further trials, testing humoral and
cellular responses, are necessary to identify possible trade-offs in
P. dominula males between two linked costly traits, mating effort
and immune function.
5.2. Studying lekking behavior: not just “child’s play”
The term lek in Swedish denotes nuptial arena of Galliform birds
but also “child’s play”: in many ways, lekking resembles a form
of behavioral play for adults. In P. dominula, hundreds of males
can be found lekking around the tops of poles, trees and other
landmarks, which may be conspicuous visually and also facilitate
pheromonal diffusion into the wind (see Table 4). Scent-marked
leaves and small perches along their patrol routes function as tiny
exclusive territories within the lek. The same lek system may be
used by sequential generations of males according to a speciesspecific temporal and spatial segregation at landmarks. There is
some evidence for alternative mating tactics, as larger males tend to
defend territories whereas smaller males spend more time searching for females in sub-optimal locations across territories, as in
other Polistes (Post and Jeanne, 1983; Polak, 1993). However, body
size is not strictly correlated with behavior, and there is a certain degree of flexibility (Beani and Turillazzi, 1988; Beani and
Zaccaroni, 2014). Because male hymenopterans lack of ornaments
and armaments, their behavioral performance becomes critical to
securing a mate. The acrobatic repetitive movements among the
same perches, following repetitive routes, may resemble for some
features the dance of manakins (Baske et al., in this issue) and be
attractive per se (Prum, 2012). Territorial males commonly mate
on their scent-marked perches, which become the cross-points of
this ‘dance’ (Beani and Zaccaroni, 2014).
The lek paradox , i.e. the conservation of genetic variation among
males, regardless of female preference for male extreme traits
(recently reviewed by Alcock and Thornhill, 2014; see Zuk and
Wedell, 2014), has probably overshadowed other components of
lekking behavior, which is widespread in insects. Leks are full of
potent visual and chemical signals and represent a changing social
context. Lekking males must be equipped by a set of sensorial and
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L. Beani et al. / Neuroscience and Biobehavioral Reviews 46 (2014) 519–533
Fig. 5. Morphological comparison of the reproductive apparatus from unparasitized (A–D) and parasitized (E–H) sexually active males of P. dominula. Stereomicrographs (A
and E) show no macroscopic difference in the apparatus: Ag, accessory gland; Sv, seminal vesicle; T, testis. Cross sections of testes (B and F) show the strong degenerative
aspects (asterisk) of the mature gonads. Semithin sections of monolayered seminal vesicles (C and G) show developed epithelial layers (Ep) surrounding a vesicle lumen
completely filled with sperm cells (Sp). Through cross sections of accessory glands (D and H), a double layer of muscle fibers (Ms) and a glandular epithelium (Ep) are visible.
The glandular lumen is full of granular secretions (Se).
From Cappa et al. (2014).
cognitive skills: spatial learning to reach the same rendezvous sites,
day after day; motor learning to patrol, mark, defend and memorize
exclusive territories; the evaluation of sexual signals and quality
of potential rivals and partners by visual/chemical cues; neural
plasticity, by continually adjusting their performance in relation
to male/female density; visual, olfactory, tactile assessments of
females before mating and male mate choice. A crowded lek may
also represent a “sensory trap” (see West-Eberhard, in this issue)
Fig. 6. On the left: males significantly (***P < 0.001) directed their choosiness toward gynes (◦ = outliers). On the right: Stepwise discriminant analysis of CHCs of 20 healthy
gynes (HG), 20 parasitized gynes (PG) and 20 workers (W) tested for male preference.
From Cappa et al. (2013).
L. Beani et al. / Neuroscience and Biobehavioral Reviews 46 (2014) 519–533
for highly gregarious future queens, which leave the colony to form
extra-nidal clusters at the end of summer (Beani et al., 2011). In this
way, males might exploit pre-existing sensory biases of females
that are attracted by wasp aggregations and by major orientation
landmarks (and thus these leks may not be “symbolic” at all, L.
Pardi pers.obs.), located along female transit routes, in areas at high
density of nests, hibernacula and foraging patches.
Who is the winner in the lek play? With regard to mating success, long-term territorial males achieve more copulations, but
records are scarce and occur mainly at the end of the nuptial season. Beani suggested the “marathoner hypothesis” (Beani, 1996)
to explain this phenomenon, which occurs in 9 out of 19 Polistes
species – specifically, that the longer a male remains at a lek, the
higher his probability of mating success. This idea is a variant of
the “endurance rivalry” hypothesis (see Table 1), an idea that has
not yet been thoroughly investigated (Andersson and Iwasa, 1996),
but recently that has received some support from studies in lekbreeding anurans (Castellano, 2009; Castellano et al., 2009). Lek
endurance may be related to energy stores. Before and after the
peak of the lek period, it is common to observe non-aggressive
Polistes males on flowering patches, covered with pollen (WestEberhard, pers. obs.). In males of P. metricus, another temperate
species, lipids and proteins significantly decrease from late summer
emergence to fall (October), whereas there is a rise in carbohydrates
due to foraging, which compensates for the loss of energy reserves
(Judd et al., 2010).
Females may use male lek persistence to select high quality
males by delaying mate selection as long as possible, until stable
leks have been established As Lloyd stressed in bumble bees and
other insects, “by scoring endurance females have a good and reliable measure of male quality” (1981); the same is likely to be true
in paper wasps. Noticeably, in the lek-like swarms of hover wasps
in the subfamily Stenogastrinae, females approached aerial aggregations at the end of the flight period, when only vigorous males
persisted in their costly displays of abdominal stripes (Beani and
Turillazzi, 1999). Waiting for a persistent male could be a parsimonious mate choice providing females with an indicator of “good
genes”.
5.3. The smart male: from the field to the lab
To the human eye, a Polistes lek looks like a cloud of insects; this
makes a difficult study subject. In addition, a bias is likely to occur
in field studies centered on the core of lek and on “hot-shot” males
(Höglund and Alatalo, 1995). An artificial lek, a large greenhouse
with paper leaves as perches and scattered resources (see Beani
and Zaccaroni, 2014), provides some real advantages, e.g. to observe
rare behaviors such as antennation, coupling and mate guarding or
the mating success of small males with well-developed AG (see
5.1, 5.2). Most importantly, observations are not biased toward the
most conspicuous territorial males.
In yet another experimental setting, observations of sexual
interactions in tiny lab arenas can provide a more detailed view
of other aspects of sexual selection, i.e. the role of male color,
abdominal spots and relatedness (see Table 4). In this simplified
environment using short-term trials, visual/chemical cues have
been implicated as important traits for mate acquisition. The yellow face and the yellow abdominal surface of males in P. dominula,
as well as the silvery hairs on the male clypeus of the polistine wasp
Chartergellus (Chavarrìa-Pizarro and West-Eberhard, 2010) and the
black pigmentation on the head of other male Polistes (de Souza
et al., 2014) might be sex-dimorphic short-range signals, a subtle
“ornament” ripe for further investigation.
It is also important not to overlook the possibility that males
exercise mate choice for females as well. In a review of sexual
selection studies on a large spectrum of species (Andersson and
529
Iwasa, 1996), female mate choice was found in 167, while male
mate choice only in 30 cases, especially when males prefer large
and fecund females. In a review devoted to insects (Bonduriansky,
2001), male mate choice was observed or inferred in 58 species
of insects, belonging to 37 families and 11 orders, although its
evidence was “sketchy” in Hymenoptera. Beyond the Darwinian
binomial “ardent males, choosy females”, in theory male mate
choice could occur also in absence of male parental care, nuptial
gifts and sex role reversal, when there is a “variation in female
quality” (Edward and Chapman, 2011; see Fig. 4).
Recent studies in P. dominula suggest males may indeed have
the ability to show mate preference between workers and future
queens (Cappa et al., 2013), i.e. castes differing in their reproductive potential (Fig. 6). The results indicated that “males do not
like the working class” (Cappa et al., 2013); they preferred gynes,
both healthy and parasitized (castrated) by X.vesparum, and this
choice was probably made on the basis of chemical cues, i.e. cuticular hydrocarbons (CHCs). Healthy and parasitized gynes are very
similar in their CHC profiles (Dapporto and Palagi, 2006; Cappa
et al., 2013), and they both possess poorly developed ovaries, large
body size and high lipid storage. These physiological similarities
could explain the males’ confusion in mate choice, in which the
parasitized females are “right” as far as their caste, but “wrong”
according to their reduced reproductive value. However, the males’
fixed amount of sperm and the large variation in female quality
should select for the evolution of male mate choice (see Fig. 4),
although this may be cryptic and difficult to quantify. Lab trials in
small arenas require some caveats and, for future studies, precautions must be made to ensure that the experimental design does not
overestimate the opportunity for male mate choice with respect to
the natural situation.
6. Wider challenges
Despite a large body of literature available for Polistes male
sexual behavior, we lack key information on how differences in
body size, mating tactics and health actually relate to the evolution of polymorphic traits, at the levels of hormones, neurons
and gene expression. As model organism, Polistes wasps offer several advantages (long-term studies on behavior and physiology,
the ability to rear and mate them in laboratory, the availability of genomic tools, see Toth et al., 2010), which make them
highly suitable to be used for pioneering work in this field. Future
research will not only add further insights into the reproductive
behavior of social hymenopterans, but also allow more general
hypotheses about the interplay between natural and sexual selection.
In wasps, bees, and ants sexually selected traits seem relatively
“weak” (Boomsma et al., 2005) both in males, devoid of armaments and ornaments, and in females, where the choice of male
traits is likely limited by ancestral monogamy and perhaps not
appreciated because of overlooked post-copulatory behaviors. By
combining quantitative behavioral data, experimental manipulation, and assessment of immune-competence in both sexes, within
and across species, it will be possible to identify shared and novel
genes involved in the expression of sexually selected traits, and to
describe co-evolved pathways of male and female phenotypes.
“Sex is an antisocial force in evolution” (Wilson, 1975). This bold
statement, which Boomsma (2007) used to introduce a review on
“kin selection versus sexual selection”, may require reconsideration. Perhaps the role of male mate choice is more important than
has previously been realized; such a revelation could imply that
male mating decisions can have a strong impact in colony life and
long-term fitness. And perhaps, thus, the ‘Ant’ could finally meet
the ‘Peacock’ (Cronin, 1991).
530
L. Beani et al. / Neuroscience and Biobehavioral Reviews 46 (2014) 519–533
Acknowledgments
We thank Stefano Turillazzi, Rita Cervo and the members of the
Florence Group for the Study of Social Insects for their assistance
during this study, both in the field and laboratory. We also thank
Ken Sasaki and Ken-ichi Harano for their hepful comments on the
neuro-endocrine section, Marlene Zuk, Mary Jane West-Eberhard
and Joan Strassmann for fruitful discussions on this review.
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