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Behavioral Ecology Vol. 10 No. 6: 641-647
© 1999 International Society for Behavioral Ecology
Facultative paternal investment in the polyphenic beetle Onthophagus taurus: the role of male morphology and social context
Department of Zoology, Duke University, Durham, NC 27708-0325, USA and Lehrstuhl Zoologie II, Theodor-Boveri-Biozentrum der Universität, Am Hubland, D-97074 Würzburg, Germany
Address correspondence to A. P. Moczek, Department of Zoology, Duke University, NC 27708-0325, USA. E-mail: armin{at}duke.edu .
Received 12 November 1999; accepted 18 April 1999.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Members of a population often differ significantly in their parental investment. Such variation is generally believed to have important consequences for mating system evolution and has been suggested to play an important role in the evolution of some secondary sexual traits and displays. Recent studies suggest that individuals are able to adjust the intensity and kind of parental investment they provide according to the breeding conditions they encounter. As a consequence, between-individual variation in parental investment may depend more on external conditions than previously thought for these taxa. This may have important implications for current perspectives on the role of differential parental investment in the evolution and maintenance of certain mating systems and sexual selection regimes. Here I quantify patterns of variation in paternal investment as a function of social conditions in a species of beetle that is dimorphic for male horn morphology. I demonstrate that under certain conditions (namely, the absence of other males), paternal assistance covaries with male morphology, with horned males investing substantially more time in assisting females than hornless males. I also show that the magnitude of differences in paternal investment between male morphs varies in response to external conditions. In the presence of other males, paternal assistance was negligible for both male morphs, who instead invested substantially and equally in mate-securing behaviors. I use my findings to discuss the significance of variation in paternal assistance for onthophagine mating systems and evaluate ideas proposed to explain the evolution of alternative morphologies in the genus Onthophagus.
Key words: beetles, facultative parental investment, honest indicators, phenotypic plasticity, polyphenism, sexual selection, Onthophagus.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Members of the same population often differ significantly in the kind and intensity of parental investment they provide for their offspring (Clutton-Brock, 1991
). Such
variation has important implications for the evolution and maintenance of
animal mating systems (Choe and Crespi,
1997a; Thornhill and Alcock,
1983) and for the intensity and direction of sexual selection in
populations (Andersson, 1994;
Choe and Crespi, 1997b).
Furthermore, certain secondary sexual traits and displays have been suggested
to have evolved in part because they reliably reflect a parent's investment
potential (Andersson, 1994;
Hunt and Simmons, 1997;
1998;
Knapp and Kovach, 1991;
Nisbet, 1973;
Sundberg and Larsson, 1994).
It has become clear in recent years, however, that the parental investment
provided by an individual needs to be recognized as a trait that can itself be
variable (Bartlett, 1987;
Dijkstra, 1986;
Moczek, 1996,
1998;
Scott, 1998a,
b;
Trumbo, 1990). Flexible
parental investment has been suggested to provide a mechanism by which a
parent can adjust the intensity and kind of parental investment it provides
according to the breeding conditions it encounters, thereby maximizing its
reproductive success under heterogeneous social and ecological conditions
(Moczek, 1998;
Scott, 1998a,
b). As a consequence, external
conditions may play an important role in determining the parental investment
an individual will provide, as well as whether individuals will differ in
their parental investment. Therefore, correct interpretation of the
significance of differential parental investment for the sexual selection
regime and the evolution and maintenance of mating systems requires a thorough
understanding of how different ecological and social conditions influence
individual parental investment, as well as knowledge of the relative
frequencies of these conditions in natural populations. Here I quantify
patterns of variation in paternal investment as a function of social
conditions in a species of horned beetle (Onthophagus taurus)
characterized by a spectacular morphological and behavioral polyphenism in
males (Moczek, 1998;
Moczek and Emlen, 1999).
Like many onthophagine species, male O. taurus express two
discrete morphologies. Males larger than a critical body size develop a pair
of disproportionately long horns on their heads, whereas males smaller than
this critical threshold develop only rudimentary horns, which results in the
co-occurrence of two discrete male morphs within populations
(Hunt and Simmons, 1997;
Moczek, 1996,
1998). Previous studies have
demonstrated that larval feeding conditions are the primary determinants of
adult body size and, by means of a threshold response, the presence or absence
of horns in males (Moczek,
1996, 1998;
Moczek and Emlen, 1999).
Earlier work showed that male horn dimorphism plays an important role in
male-male competition over mates. Horned males rely exclusively on aggressive
fighting behaviors to gain and maintain access to females, whereas hornless
males engage in nonaggressive sneaking behaviors when confronted with
physically superior males (Moczek,
1996).
Like many coprophagous beetles, O. taurus adults provision dung
for their offspring in tunnels excavated underneath dung pads
(Halffter and Edmonds, 1982).
Dung fragments are transported to the blind end of these tunnels and formed
into compact brood balls. At the top end of each brood ball an egg chamber is
formed, provided with a single egg, and sealed with an excrement cap. No
further care is given to the offspring, and each brood ball constitutes the
total quantity of food available to a single larva
(Goidanich and Malan, 1962,
1964;
Moczek, 1996). Competition for
both dung and matings is likely to be severe in field populations, as O.
taurus densities in single dung pads often exceed 100 individuals and
dung pads are patchy and short-lived resources
(Moczek, 1996, unpublished
data; see also Emlen, 1994;
Halffter and Edmonds, 1982;
Hanski and Cambefort,
1991).
Several studies have indicated that males and females cooperate in the
process of brood ball production (Emlen,
1994; Hunt and Simmons,
1998; Moczek,
1996) and that male assistance can increase the number of brood
balls a female can produce (Cook,
1988; Rasmussen,
1994; Sowig,
1996b). Alternatively, male assistance may result in an increase
of the average size of brood balls produced by a female
(Cook, 1988;
Hunt and Simmons, 1998). Brood
ball size is an important determinant of larval development, adult body size,
and male horn phenotype (Hunt and Simmons,
1997; Moczek,
1998; Moczek and Emlen,
1999). Although the fitness consequences of increased brood ball
weight are not fully understood, recent studies argued that an increase in
average brood ball size due to male assistance improves female fitness via the
production of offspring of higher reproductive value
(Hunt and Simmons, 1997,
1998). If males differ in
their potential to assist females, this should favor female preferences for
males with high investment potential, provided signals exist that reliably
indicate a male's ability to assist a female. Using breeding experiments, Hunt
and Simmons, (1998) found,
contrary to expectations, that female O. taurus paired with either
horned or hornless males produced fewer brood balls compared to females
breeding alone. However, they also observed that females paired with horned
males produced brood balls that were significantly heavier than brood balls
produced by females paired with hornless males or females alone. They
concluded that breeding with horned males confers a reproductive advantage to
females and raised the possibility that horn evolution may in part have been
driven by female choice for the benefits of paternal investment that horns
signal (Hunt and Simmons,
1998).
Variable degrees of competition for resources and mates are important
aspects of onthophagine mating systems
(Emlen, 1994,
1997;
Moczek, 1996,
Moczek and Emlen, 1999), and
onthophagine beetles show a remarkable degree of adaptive plasticity in both
male and female breeding behavior (Moczek,
1996, 1998;
Sowig, 1996a). I explored
paternal investment of horned and hornless O. taurus as a function of
the social conditions encountered by the investing individual. Using direct
observations of male underground behavior, I estimated paternal investment of
both morphs in the absence and in the presence of potential competitors. I
used the proportion of time invested in cooperative versus mate-securing
behaviors as an estimate of paternal assistance. I use my findings to discuss
the significance of variation in paternal assistance for onthophagine mating
systems and refine recent ideas proposed to explain the evolution of
alternative morphologies in the genus Onthophagus.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Onthophagus taurus is a common dung beetle in open pasture land in North Carolina. O. taurus became introduced to the United States by accident, probably in the late 1960s, and was first recorded in Santa Rosa County, Florida, in 1971 (Fincher and Woodruff, 1975
). O. taurus has continuously extended its
range since then and now represents the dominant onthophagine species in open
pasture land in North Carolina (Moczek,
1996, 1998).
Beetles used in these experiments were collected as adults from a pasture near
Durham, North Carolina, and maintained on cow manure in the laboratory (for
details on O. taurus's natural history, see
Moczek, 1996,
1998,
Moczek and Emlen, 1999).
Underground observations
To observe underground behavior, I constructed ant farms consisting of 25
x 35 cm glass panes separated by a 4-mm wide U-frame made of plywood.
Horizontal PlexiglasTM panes were constructed to fit over these farms to
allow beetles to walk freely on this surface once they chose to leave the
farm. Ant farms were filled three-quarters full with a sand/soil mixture, and
the remaining space was filled with dung. Additional dung was provided on the
Plexiglas surface. Because tunneling behavior naturally occurs in darkness, I
conducted all behavioral observations in a darkroom using only red filtered
light. In all experiments beetles tunneled readily into the space provided by
the ant farm, engaged in courtship and mating, and produced brood balls and
oviposited, suggesting that the farms used in this study effectively imitated
natural conditions of O. taurus (design followed suggestions in
Emlen, 1993,
1997).
Classification of male behavior
Qualitative behavioral observations were used to define types of behavior
displayed by male O. taurus. Males engaged in seven clearly
recognizable types of behavior during the process of tunneling and brood ball
production: (1) tunneling: removal of soil with front legs, pushing of soil
tunnel upward using either abdomen or prothorax; (2) acquisition and transport
of dung: removal of dung fragments from the pad with dung fragments either
held by front legs and pulled, pushed using the prothorax, or dropped through
steep parts of the tunnel; (3) tunnel blocking: male remains motionless inside
the tunnel close to, and facing, the tunnel entrance; usually displayed while
female is below the male and after contact with other males; (4) patrolling:
male runs quickly down the tunnel, remains inside the brood ball for a few
seconds, and proceeds quickly back to the tunnel entrance, both times without
carrying dung or soil with him, (5) guarding the female: male stays in close
proximity to the female's head or abdomen (<1 cm) and initiates frequent
body contact with his front legs and antennae but does not assist the female;
(6) mating: time spent in copula; (7) eating: dung fragments are held in front
of the head while mouth parts move frequently. Male behavior was scored as not
classified if it did not fit any of the above definitions or if only certain
aspects of a behavior category were displayed. For example, males in close
proximity to a female but without displaying frequent body contact were not
scored as guarding the female (for detailed description of each type of
behavior, see Moczek,
1996).
I quantified the behavior of horned and hornless male O. taurus after exposing them to two experimentally controlled situations: both morphs were given access to a female either alone (noncompetitive situation) or in the presence of a second male (competitive situation).
Quantification of male behavior
Non-competitive situation
I placed a randomly selected, field-caught female in an ant farm and
provided her with dung. Tunnel digging usually occurred within 2 h, then
either a horned or hornless male was added. I allowed the pair to adjust to
the situation for an additional 2 h and then observed them for a minimum of
three 30-min periods distributed over the course of the next 24 h. All
behavior displayed by both male and female were recorded in 30-s intervals
using instantaneous scan sampling (Martin
and Bateson, 1993). I used the total number of intervals during
which a male was scored as displaying a particular type of behavior to
calculate the proportion of time (relative to the total time observed) that a
male invested in this particular behavior. I conducted this experiment for a
total of 12 males of each morph. All individuals were only used once.
Competitive situation
Ant farms were set up as described above. After introducing either a horned
or hornless male and a subsequent accommodation period of 2 h, I added a
second male. Contact between males was ensured by placing the second male head
first in the tunnel occupied by the first male. In all cases beetles ran down
the tunnel and encountered the previously introduced male, which always
resulted in fights between males until one of them was defeated. I then
recorded the behaviors of the dominant male and the female for at least three
30-min periods as described above. Behavior of the defeated male was recorded
qualitatively.
Previous work demonstrated that hornless males are unable to win fights and
cannot maintain residency inside a tunnel in competition with a horned (and
therefore physically larger) male (Moczek
and Emlen, 1999). Therefore, I was not able to randomly select the
second male added to a farm for those experimental trials involving hornless
males as focal males. Because one aim of this experiment was to quantify
patterns of horned and hornless males' assistance to a female in the presence
of potential competitors, I had to ascertain that, in spite of the presence of
a second male, a hornless male remained resident inside a tunnel and thus
maintained at least the option to assist the female. The only way to achieve
this was by using only hornless males as opponents if the focal male was
himself hornless. For trials involving horned males as focal males, competing
males were selected randomly. I conducted this experiment for 10 males of each
morph. Individuals were only used once.
Duration of copulation
O. taurus courtship behavior consists of the male drumming his
forelegs over the back and sides of the female until the female moves into a
position appropriate for intromission (see also
Emlen, 1994;
Moczek, 1996). Drumming stops
immediately with intromission. Copulation is terminated by the female either
by running down the tunnel and dragging the male behind her for a short
distance, or by using her hind legs to slip off the male. Hence, copulation
duration is clearly definable. I observed more than 120 matings and measured
copulation durations of 83 males including both male morphs in noncompetitive
as well as competitive situations. Durations were measured to the nearest
second using a stop watch. In nine cases I measured two copulation durations
of the same individual male (mean variation between measurements: 22 s). In
these instances I used the individuals' mean copulation duration for
analysis.
Statistical analysis
Males assisted females in the process of brood ball production via
tunneling and the acquisition and transport of dung fragments down the tunnel.
I calculated the proportion of time (i.e., relative to the total time
observed) that a male invested in these particular behaviors and used the
combined proportion as an estimate of a male's investment in cooperative
behavior. Analogously, I calculated the proportion of time invested in
blocking, patrolling, and guarding and used the combined proportion as an
estimate of a male's investment in mate-securing behavior. The time spent
eating was generally brief in all trials and was excluded from the analysis.
Mating durations were analyzed separately (see below). I compared male
investment in cooperative versus mate-securing behavior as a function of male
morphology (horned versus hornless) and the behavioral context (competitive
versus non-competitive situations) using nonparametric Mann-Whitney U
tests (Sachs, 1992). I used
t tests to compare copulation durations of horned and hornless males
in both behavioral contexts. All significance levels reported below, including
both parametric and nonparametric tests, were corrected for multiple
comparisons using sequential Bonferroni corrections where necessary
(Sachs, 1992;
Sokal and Rohlf, 1995).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Male investment in the absence of competitors
Horned and hornless O. taurus differed substantially in the amount of time spent assisting females (Figure 1; unless otherwise noted all data are shown as means with standard deviations in parentheses). Horned males were observed either excavating or transporting dung for 56% (20.4) of the time observed, whereas hornless males were only observed to invest 12% (5.8) of the time observed in these behaviors (n = 12 each, p <.01). Instead, hornless males spent considerably more time blocking the tunnel entrance, patrolling, and guarding the female than did horned males [horned males: 13% (11.5), n = 12; hornless males: 50 (19.8), n = 12, p <.01].
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Male investment in the presence of competitors
Horned and hornless males did not differ in their allocation of time to
particular behaviors when an additional male was present
(Figure 1). Both morphs
invested an almost equal proportion of time in mate-securing behaviors [horned
males: 72% (21), n = 10; hornless males: 69% (18), n = 10,
p >.5], and relatively little in cooperative behaviors [horned
males: 5% (4.8), n = 10; hornless males: 7% (7.5), n = 10,
p >.3].
Comparing time allocation across both social situations (presence versus absence of additional male) indicated that both male morphs invested significantly more time in matesecuring behaviors when an additional male was present [horned males: no additional male: 13% (11.5), n = 12 versus additional male present: 72% (21), n = 10, p <.01; hornless males: no additional male: 50% (19.8), n = 12 versus additional male present: 69% (18), n = 10, p <.05; Figure 1]. In horned males, increased investment in these behaviors was clearly at the expense of cooperation with the female [time spent cooperating in the absence of other males: 56% (20.4), n = 12; in the presence of other males: 5% (4.8), n = 10; p <.01]. Hornless males appeared to respond in a similar, albeit much less dramatic, fashion to the presence of potential competitors [time spent cooperating in the absence of other males: 12% (5.8), n = 12; in the presence of other males: 7% (7.5), n = 10, p <.05 before Bonferroni correction, not significant after Bonferroni correction]. The time spent eating did not differ as a function of male morphology or behavioral context (not shown).
Duration of copulation
Horned males copulated significantly longer than hornless males, both in
the presence and absence of additional males [no additional male: horned males
146 s (26), n = 24, hornless males 104 s (18), n = 23,
p <.01; additional male present: horned males 104 s (22),
n = 18, hornless males 82 s (21), n = 18, p
<.01; Figure 2]. Although
the difference between morphs was significant both in the presence and absence
of additional males, both male morphs exhibited significantly shorter
copulation durations when an additional male was present (p <.01
for each comparison; Figure
2).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Paternal investment in dung beetles has long been recognized, although its implications continue to be debated (e.g., Cook, 1988
;
Goidanich and Malan, 1964;
Halffter and Edwards, 1982; Hunt and
Simmons, 1998; Rasmussen,
1994). In this study I demonstrated that, under certain
conditions, assistance by male O. taurus covaries with male
morphology (see also Cook,
1988; Emlen, 1994,
1997;
Hunt and Simmons, 1998; but
see Rasmussen, 1994). Horned
males invested considerably in tunnel excavation and transport of dung into
tunnels, whereas hornless males exhibited comparatively little investment in
these behaviors and instead engaged in mate-securing behaviors. However,
differential paternal assistance depended on the absence of potential
competitors. Paternal investment in cooperative behaviors was negligible for
both male morphs when competitors were present, and instead both morphs
allocated most of their time to mate-securing behaviors. Most previous studies
on paternal assistance in dimorphic scarab species examined male cooperation
without varying the social conditions (e.g.,
Cook, 1988;
Hunt and Simmons, 1998,
Rasmussen, 1994; but see
Emlen, 1994). Thus, whether
faculatative paternal assistance is restricted to O. taurus or a more
general component of dung beetle mating systems remains to be shown.
Interestingly, Emlen's (1994)
study on the congener O. acuminatus entailed examination of male
assistance in the presence and absence of other males but did not find any
indication that males adjust their behavior accordingly.
Evolution of facultative paternal assistance in dung beetles
Competition for breeding opportunities in the field is intense in many dung
beetle communities, as dung pads are patchy and often short-lived resources
(Halffter and Edmonds, 1982;
Hanski and Cambefort, 1991).
In North Carolina O. taurus densities in single dung pads typically
exceed 100 individuals, and dung pads often dry out (and hence can no longer
be used for brood ball production) in less than 24 h
(Moczek, 1996, personal
observation). Assisting a female in using such an ephemeral resource appears
adaptive because it may allow a female to produce a greater number and size of
brood balls within a given amount of time and hence would allow the male to
sire a greater number of offspring (e.g.,
Cook, 1988;
Rasmussen, 1994).
Earlier work suggested that, besides competition for dung, intense
male-male competition for females may also be an important determinant of male
fitness and that males have evolved alternative reproductive tactics to access
females (Moczek, 1996;
Moczek and Emlen, 1999).
Horned males rely exclusively on aggressive fighting behaviors to gain and
maintain access to females in breeding tunnels, whereas hornless males engage
in nonaggressive sneaking behaviors when confronted with physically superior
males (Moczek, 1996;
Moczek and Emlen, 1999). These
studies also indicated that tunnel possession is crucial for gaining mating
opportunities, as matings almost exclusively occur inside tunnels, and the
male in possession of a tunnel is likely to be the last male mating before
oviposition (Moczek, 1996;
Moczek and Emlen, 1999).
Studies on the alternative reproductive tactics of O. taurus
(Moczek, 1996) and O.
acuminatus (Emlen, 1994,
1997) revealed that males who
leave tunnel entrances to assist in dung acquisition or to dispose of
excavated material are particularly vulnerable to sneaking by other males, who
can temporarily gain access to the female and mate with her, or to losing
tunnel ownership altogether. Therefore, although paternal assistance is likely
to increase male reproductive success via increasing the number and weight of
brood balls a pair can produce, it entails the cost of putting tunnel
possession, and thus current and future mating opportunities, at risk. It
therefore would appear adaptive for resident males to reduce cooperative
behaviors in the presence of other males and instead to allocate more time to
mate securing behaviors such as guarding.
The present study suggests that both horned and hornless male O.
taurus are indeed able to recognize the presence or absence of other
males and respond by adjusting their investment into cooperative versus
mate-securing behaviors accordingly. Such condition-dependent paternal
assistance may represent a mechanism by which males maximize fitness in a
social environment composed of variable degrees of male-male competition for
females. Facultative parental investment may be particularly likely to evolve
if a patchy and ephemeral resource environment favors cooperation, while at
the same time intraspecific mating competition selects for behaviors that
secure mates and breeding opportunities (see also
Scott, 1998a,
b;
Trumbo, 1991;
Trumbo and Fernandez, 1995).
Such ecological and social conditions are not uncommon (e.g.,
Choe and Crespi, 1997a,
b), and condition-dependent
parental investment may be more widespread than currently recognized.
The evolution of alternative paternal investment
Several studies on paternal assistance in dimorphic scarab species found
evidence that horned (major) males invest considerably more time in assisting
females than hornless (minor) males (Cook,
1988; Hunt and Simmons,
1998; Emlen, 1994;
but see Rasmussen, 1992,
1994). Although cooperation in
horned males appears adaptive as it is likely to increase a pair's efficiency
to use an ephemeral resource, the lack of assistance by hornless males appears
maladaptive at first sight. However, not assisting a female may in fact
increase a hornless male's fitness if this permits him to locate and mate with
other females. Although this behavior would entail the risk that other males
may displace his sperm in abandoned females, this risk may be outweighed by
opportunities to inseminate additional females, provided such additional
mating opportunities are indeed available
(Parker, 1970,
1974; see below). Why then do
horned males generally stay, assist females, and defend tunnel entrances?
Earlier work suggests that the possession of horns, albeit beneficial in
direct combat, reduces male maneuverability inside breeding tunnels
(Emlen, 1994;
1997;
Moczek, 1996). For example,
horns scrape against tunnel walls as beetles run below ground and impede a
horned male's ability to turn around inside tunnels
(Moczek, 1996). In contrast,
hornless males appear well equipped to move quickly inside tunnels and to
acquire mating opportunities even in the presence of guarding males
(Emlen, 1997;
Moczek, 1996). Earlier work
conducted on O. taurus males of similar body size with different horn
lengths demonstrated that short-horned males moved significantly faster
through standardized tunnels than their long horned counterparts
(Moczek, 1996). As a
consequence, it may be more difficult for horned males to effectively access
multiple females in dung pads, and staying with a female, assisting her, and
defending a once acquired residency inside a tunnel may present the tactic
with the highest fitness gain for horned males.
Whether hornless males can indeed maximize their fitness by locating and
mating with multiple females while minimizing their investment into
cooperative behaviors would critically depend on the availability of
additional females (see also Carroll,
1991, 1993;
Carroll and Corneli, 1995;
Parker, 1970,
1974;
Shivashankar and Pearson,
1994). As a single dung pad may contain more than 100 O.
taurus individuals, the probability that a male will succeed in locating
multiple females in the same pad appears high. In contrast, in species with
low population densities, hornless males may not always have the option to
locate additional females. In this case, hornless males might be predicted to
maximize their fitness by behaving like horned males (i.e., to stay with a
female and to cooperate in the process of brood ball production).
It is worth noting that correlations between a male's assistance potential
and horn morphology have so far been documented in three species that all
exhibit extremely high field densities of several hundred individuals per
single dung pad (O. binodis:
Cook, 1988;
Ridsdill-Smith and Hall, 1984;
Ridsdill-Smith et al. 1982;
O. taurus: Dadour et al.,
1999; Hunt and Simmons,
1998; Hunt et al.
1999; Moczek,
1996; this study; O. acuminatus:
Emlen, 1994;
1997;
Howden and Young, 1981). The
only study in which both horned and hornless males did not differ in their
investment in cooperative behaviors was conducted on the horned rainbow scarab
Phanaeus difformis (Rassmussen,
1994). In this species natural dung pads typically attract 5-10
beetles (Rasmussen, 1992),
resulting in densities 1-2 orders of magnitude lower than in any of the 3
onthophagine species (see also Blume and
Aga, 1976; Fincher et al.,
1986). I expect that further integration of population structure
and demography into studies on alternative and facultative paternal assistance
will provide interesting insights into how social and ecological environments
shape individual behavior in dung breeding beetles.
Implications of facultative paternal care: male morphology as a
reliable signal
A number of studies have demonstrated that the presence of males correlates
either with an increase in the number of brood balls produced
(Cook, 1988;
Rasmussen, 1994;
Sowig, 1996b) or an increase
in average brood ball weight (Hunt and
Simmons, 1998) and may therefore increase parent fitness. Several
studies have also investigated paternal investment in dung beetles that are
dimorphic for male shape (Cook,
1988; Emlen, 1994,
1997;
Hunt and Simmons, 1998). Cook
(1988) found that O.
binodis females paired with horned males produced a greater number of
brood balls than females paired with hornless males or single females. In
contrast, Hunt and Simmons
(1998) found that O.
taurus females paired with males of either morph produced significantly
fewer brood balls than single females and suggested that the time paired
females spent mating instead of building brood balls accounted for this
observation. However, they also observed that females paired with horned males
produced significantly heavier brood balls than any other treatment group.
Although the fitness consequences of the production of heavier brood balls
remain to be quantified, both Cook and Hunt and Simmons interpreted their
findings as a reflection of higher levels of assistance in horned males and
suggested that the possession of horns may serve as an indicator of a males'
cooperation potential (Cook,
1990; Hunt and Simmons,
1998). Consequently, Hunt and Simmons
(1997,
1998) suggested that horn
evolution may in part be driven by female choice for the benefits of paternal
investment that horns signal.
The present study may help to refine this notion. Both Cook
(1988) and Hunt and Simmons
(1998) used the number and
weight of brood balls produced by multiple males and females in
single-breeding containers as an indirect estimate of relative paternal
investment (Cook—three treatments: two horned males per female, two
hornless males per female, and single females; Hunt and Simmons—four
treatments: six horned males + six females, six hornless males + six females,
three horned + three hornless males + six females, and six females without
males). Here I demonstrated that males respond to the presence of other males
by engaging in matesecuring behaviors at the expense of cooperation. In many
observations the resident male had to interact only once with the second male
introduced to an ant farm to terminate cooperative behavior for the entire
observation period. Furthermore, pilot observations revealed that both male
morphs try to mate with as many females as are tunneling in a container or ant
farm, abandoning the female they originally assisted and interfering with
brood ball production of neighboring pairs
(Moczek 1996, unpublished
data). Comparing the breeding success of unpaired females with the breeding
success of multiple males and females in single-breeding containers may
therefore not be a meaningful estimate of relative male assistance potential,
as it confounds possible contributions of individual male behavior and
male-male interactions to breeding success. Male interference with brood ball
production of neighboring pairs may also explain why Hunt and Simmons
(1998) found that single
females produced a larger number of brood balls than females paired with males
of either morph, a result that was not found using single pairs and single
females (Moczek and Scott, unpublished data).
The hypothesis that male horn morphology may serve as an indicator of
paternal quality nonetheless remains interesting. The present study shows that
in the absence of other males, horned males allocate a substantially larger
amount of time to cooperative behaviors than hornless males. Under these
conditions horn expression may indeed have the potential to reliably signal a
males' assistance potential, and females may be expected to express a
corresponding preference under such circumstances. So far, however, there is
no evidence that females discriminate among morphs. In all experiments and
behavioral observations females appeared to mate readily with both male morphs
(see also Moczek and Emlen,
1999). However, early termination of copulations may provide a
mechanism by which females exert cryptic choice
(Eberhard, 1996). The
differences in copulation durations between male O. taurus morphs are
consistent with this view (Figure
2). Horned males copulated significantly longer than hornless
males. This difference persisted in the presence of other males, although,
interestingly, both morphs exhibited reduced copulation durations under these
conditions.
Alternatively, differences in copulation duration may simply be a
reflection of variation in copulatory properties of both morphs and therefore
may indicate sperm competition between males rather than discrimination by
females (Simmons et al.,
1999). In a recent study, Simmons et al.
(1999) found that in O.
binodis, large, horned males develop relatively smaller testes and
produce relatively smaller ejaculate volumes than hornless males. This
suggests that large, horned males may simply require more time to release the
same amount of sperm, which may explain differences in copulation durations
between morphs observed in the present study. However, Simmons et al.
(1999) did not find a
corresponding correlation between male morphology, testes size, and ejaculate
volume for O. taurus, which suggests that additional factors may be
important in determining copulation durations in this species.
Although the possible signaling function of horns in horn dimorphic species
remains an intriguing possibility, it is important to note that, at least in
O. taurus, any correlation between male horn expression and the
extent of paternal assistance disappears in the presence of additional males
(see (Figure 1). In O.
taurus and many other horn dimorphic dung beetles, competition for both
dung resources and mates is severe in field populations (see above). Assisting
a female in the absence of competing males may therefore not be an option for
most males most of the time, regardless of male morphology. Although there is
substantial evidence that supports the view that horns and horn dimorphisms
have evolved and are maintained in the context of male-male competition, any
association between horn possession and signaling of paternal quality remains
to be demonstrated (e.g., Eberhard,
1978, 1979,
1981,
1982,
1987;
Emlen, 1997;
Moczek, 1996;
Moczek and Emlen, 1999;
Otronen, 1988;
Palmer, 1978;
Rasmussen, 1994;
Siva-Jothy 1987).
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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This paper benefited from the constructive comments and suggestions by two anonymous reviewers. M. Beebee, L. Mojonnier, C.P. Klingenberg, and H.F. Nijhout provided helpful comments on previous versions of the manuscript. I also thank L.W. Simmons, J.L. Tomkins, and J. Hunt for helpful discussions and for making their unpublished results available to me. I am grateful to K. Fiedler, D. Emlen, P. Klopfer, and B. Hölldobler for valuable advice and support during the course of this study. P. and M. Klopfer kindly allowed me to collect beetles on their pastures. This work was carried out while I was funded by a scholarship by the German Academic Exchange Service (DAAD).
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