ALLEN J. MOORE* .... observations were made under dim red light. ..... domestic dogs, Canis familiaris (Scott & ..... Reich, T., James, J. W. & Morris, C. A. 1972.
Anita. Behav., 1990,39, 388-397
The inheritance of social dominance, mating behaviour and attractiveness to mates in male Nauphoeta cinerea A L L E N J. M O O R E * Institute for Behavioral Genetics, and Environmental, Population, and Organismic Biology, University of Colorado, Boulder, CO 80309-0334, U.S.A.
Abstract. In the cockroach Nauphoeta cinerea, male social behaviour is influenced by sexual selection due
to mate choice by females for dominant males. This paper reports the results of breeding experiments in N. cinema that document genetic variation in (1) male dominance rank, (2) components of courtship associated with differences in dominance rank and important in male mating success, and (3) male attractiveness to females. Dominant males typically produced offspring that were dominant in social interactions as adults; subordinate males produced subordinate offspring. Estimates of narrow-sense and broad-sense heritabilities of sexually selected male courtship behaviour indicated that moderate to high additive genetic variation persists despite sexual selection. Estimates of genetic correlations for different c~omponents of courtship and mating suggested similar genetic influences and that these components reflect male attractiveness to females. In addition to the variability in the length of interactions leading to copulation, some males were consistently rejected as mates. Male attractiveness to females was therefore a threshold character with two levels of expression; this acceptance/rejection threshold was also heritable. These results are consistent with studies of sexually selected morphology and suggest that there may be general patterns involved in the genetics of sexually selected traits.
A renewed interest in sexual selection has led to its implication in shaping the evolution of a wide variety of social behaviours (Blum & Blum 1979; Smith 1984; Eberhard 1985). Empirical studies of the mechanisms of sexual selection, male-male competition and especially female mate choice, have been numerous in recent years. Although studies that separate and document the existence of these mechanisms are a necessary first step, and often the only study that can be performed with many species, they are also incomplete (Endler 1986; Grafen 1988). Several other aspects of sexual selection have not been adequately addressed. Genetic studies of sexual selection are particularly lacking (Bateson 1983; Bradbury & Andersson 1987; Kirkpatrick 1987). In most previous studies of sexual selection, like many evolutionary studies of behaviour, the necessary genetic variation was assumed to be, or have been, present. This assumption of persistent genetic variation has been questioned for traits that experience sexual selection. Theoretical considerations have suggested that heritable variation should not be *Present Address: Department of Anatomy and Neurobiology, Washington University School of Medicine, Box 8108, 660 S. Euclid Avenue, St Louis, MO 63110, U.S.A. 0003 3472/90/020388+ 10503.00/0
present in characters that influence mate choice (Williams 1975; Maynard Smith 1978), since genetic variation should be lacking in characters that are closely related to fitness (Fisher 1958; Falconer 1981). This prediction presents a major challenge to sexual selection theory: why should females discriminate among mates that do not vary genetically (West-Eberhard 1979; Thornhill & Alcock 1983; Heisler 1984)? Although mechanisms have been proposed that may maintain additive genetic variation in sexually selected traits (Arnold 1983; Cade 1984; Bradbury & Andersson 1987), empirical genetic studies are clearly necessary to clarify the importance of these challenges to modern sexual selection theory (Bradbury & Andersson 1987). Selection, however strong, will not result in evolution in the absence of heritable variation (Lande & Arnold 1983). Contrary to theoretical predictions, the few empirical investigations have documented significant additive genetic variation in traits important in mate choice. Most of these studies have focused on morphological characters (Carson 1985; Houde 1987; McClain 1987; Simmons 1987). There has been one study of sexually selected behaviour: cricket calling-bout length (Hedrick 1988). There have been no investigations of the inheritance of
9 1990The Association for the Study of Animal Behaviour 388
Moore: Inheritance of sexually selected behaviour
sexually selected social behaviour in organisms with dominance hierarchies. This is unfortunate since many contentious aspects of sexual selection, especially when mate choice is not resource based, involve considerations of female choice for dominant males (Borgia 1979; Taylor & Williams 1982; Borgia et al. 1985). I therefore investigated the possibility that sexually selected social behaviour is inherited, and that additive genetic variation exists, despite a mating preference for dominant males. This study was conducted on Nauphoeta cinerea, a cockroach species in which mating behaviour and sexual selection are well documented (Moore & Breed 1986; Moore 1988, 1989). Here, I report the results of breeding experiments that examine the genetic basis for variation in (1) male ability to dominate in intrasexual social interactions, (2) male courtship behaviour and (3) male acceptability as a mate. Since females preferentially mate with dominant males (Breed et al. 1980; Schal & Bell 1983), these acts reflect the differences among males that modify female mate choice (Moore & Breed 1986; Moore 1988; Moore & Moore 1988).
MATERIALS
AND METHODS
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Plexiglas mating cage measuring 27 x 15 x 13 cm. This mating cage held over 100 males that had been isolated prior to adult eclosion and had subsequently reached sexual maturity. All males in these cages were between 9 and 21 days post-adult moult and all females were between 7 and 15 days postadult moult. These ages represent periods of maximum and consistent sexual activity (Roth & Barth 1967). Four to seven females were placed in the mating cage simultaneously and left with males for 24 h. Females were then removed, put into individual cages and allowed to give birth. These procedures were intended to yield offspring that reflect matings that occur in unmanipulated stock colonies. First generation (F 0 males were produced by mating one female from the stock colonies (isolated as above) with a P~ male of known dominance rank. Both P1 and F~ generations were obtained from the first clutch produced by females. Since N. cinerea females mate with only one male prior to producing the first clutch (Roth 1962, 1964), this assured that all the offspring within a family were sired by the same male.
Behavionral Observations Social dominance
Rearing Methods Cockroaches for these experiments were obtained from laboratory stocks maintained at the University of Colorado. The general rearing procedures for these stocks are described elsewhere (Breed et al. 1980; Moore & Breed 1986). Specific procedures for these experiments follow those developed in previous studies of sexual selection in N. cinerea (Moore & Breed 1986; Moore 1988; Moore & Moore 1988). Cockroaches were maintained in the laboratory at 25-27~ under a 12:12 h light:dark cycle. All individuals were provided with food and water ad libitum. Individuals used in the tests were isolated at the last instar nymph stage, and both males and females were isolated from adult males to control for learning of social cues (Moore 1988, 1989; Moore & Moore 1988). Behavioural observations were made under dim red light. Generation o f P 1 and F 1 stocks
Parental generation (P0 males were obtained from females mated to males of unknown status; these females had been removed from stock colonies prior to adult eclosion. The females were placed in a
Dominance rank in males was scored on the basis of agonistic behaviour. Agonistic interactions among males and the formation of dominance hierarchies are described in detail in Ewing (1972), Bell & Gorton (1978) and Moore ct al. (1988). Dominant males typically initiate agonism; dominant males lunge, butt, kick, grapple and bite while subordinate males crouch and retreat (Bell & Gorton 1978). When all of the males in the hierarchy are the same age and are socially naive prior to placement in the group, dominance relationships are stable for at least 2 weeks (Moore et al. 1988). Most interactions in stable hierarchies involve lunging by the dominant male and retreating by the subordinate male. The most dominant individual is also the most active male in the hierarchy. In these experiments, groups of either four or two males were observed for 10 min, a period of time sufficient for stable relationships (no reversals) to develop (Moore et al. 1988). All agonistic acts described by Bell & Gorton (1978), and all interactions, were recorded. Within each group all males were matched for age (within 1 day). Dominance rank was scored 10 days post-adult eclosion. Prior to adult eclosion, P1 were removed
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from their family group and placed into individual 0.4-1itre cardboard containers. This procedure ensured that the males were never exposed to other adult males. Dominance rank was determined by placing two randomly chosen isolated males together into a Plexiglas cage measuring 27 x 15 x 13 cm and recording all agonistic interactions. Males were retested the following day: only pairs with repeatable outcomes were used in further experiments. F~ males were also removed from family groups prior to adult eclosion and maintained in individual containers like the P1 males. The dominance rank of F~ males was scored at 10 days post-adult eclosion using the same methods employed in the P: generation. Mating behaviour
Courtship in N. cinerea follows a predictable sequence (Roth 1964; Moore & Breed 1986). Females are first attracted from a distance (prior to the female contacting the male with her antenna) by a sex pheromone emitted by the male and produced by sternal glands on the abdomen (Roth & Dateo 1966; Sreng 1984, 1985). Once a female contacts a male, the male responds by initiation courtship and interactions are influenced by a non-volatile pheromone produced by dorsal glands in the male (Sreng 1984, 1985). Courtship begins when the male faces away from the female and raises his wings. The female then climbs up on the male's abdomen and palpates the male's dorsal surface. After the female climbs on the male's back, he begins to probe the ventral surface of the female's abdomen attempting to engage his phallomere. Copulation begins when the male successfully grasps the female and an end to end position is adopted. After copulation the female remains quiescent next to the male for a short period. The courtship of this species can therefore be described by six quantifiable behavioural acts: (1) speed of attraction, the length of time until a female contacts the male; (2) speed of the wing-raise response, the amount of time from the female contact until the male initiates courtship; (3) speed of the climb response, the length of time from the initiation of male courtship to the female response; (4) courtship speed, the total amount of time spent by a male courting the female, i.e. from the approach of a female to the initiation of copulation; (5) length of copulation, the amount of time the male and female are in the end to end position; and (6) length
of post-mating association, the amount of time a female remains quiescent next to a male after copulating (Moore & Breed 1986). The duration of each act is measured in seconds. Mating behaviour was studied by placing either a P1 or a F 1 male and ohe female into a clean 27 • 15 • 13 cm mating arena as in previous studies (Moore & Breed 1986; Moore & Moore 1988). Variation in the duration of the components of courtship was compared among males of different dominance rank that had courtship terminated with a normal mating. The courtship and mating of 45 P: males of known status was observed. Mated females were then placed into individual cages to give birth to first generation offspring. Two females were lost before offspring were produced. Courtship and mating of Fa males was observed until a complete mating sequence, including copulation, was obtained for three brothers per family. Behavioural measures were log-transformed prior to regression or ANOVA. Attractiveness to mates
Although mating with most males occurred soon after the female contacted the male (hereafter called accepted males), a small proportion of males in this population had mating attempts rebuffed by females (called rejected males). In interactions with rejected males, females refused repeated copulation attempts by the male, although the behaviour of both the male and the female prior to copulation attempts (from the approach of the female through the attempted copulation by the male) did not differ from male-female interactions in successful copulations. Males that were rejected remained unmated even though females were left in the cage with the male for up to 30 min. Different virgin females were placed with each rejected male (usually on successive days but no more than two females per day) to confirm a rejected mating. Successful matings with rejected males were eventually achieved by leaving a female with the male over several days. Scores for rejected males (P1 N = 9 , all from different families) were not included in calculations ofheritabilities of courtship behaviour. Inheritance
In each experiment, inheritance is demonstrated by documenting the resemblance between fathers
Moore: Inheritance of sexually selected behaviour and sons. Where possible, standard quantitative genetic techniques were used (Falconer 1981). In all experiments, the influence of shared environment between fathers and sons was eliminated experimentally. Thus, any resemblance across generations can be attributed to genetic effects.
Social dominance In the genetic analysis of dominance rank, I scored males as either dominant or subordinate based on pairwise comparisons of previously socially naive adult males. Test groups were formed by placing an offspring of a dominant male parent with an offspring of a subordinate male. Comparisons were made between different families from those paired in the P1 generation; e.g. if male A was subordinate to male B, his offspring were tested against males with a parent other than B.
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is expressed only when a threshold is exceeded (Falconer 1981). The heritability of liability therefore describes the extent to which the variation in the expression of a trait (exceeding the threshold) is due to genetic differences among individuals. Im & Gianola (1988) argue that heritabilities of binary traits can be estimated without assuming an underlying normally distributed liability or a threshold. The method o f I m & Gianola uses the more familiar parent-offspring regression. This measure describes the extent to which the likelihood of falling in one of the two classes is due to genetic differences among individuals.
RESULTS Inheritance of Ability to Socially Dominate
I estimated heritabilities and genetic correlations of courtship components. The heritability of a trait describes the proportion of phenotypic variation than can be attibuted to genetic differences among males within a population (Falconer 1981). A genetic correlation or covariance describes the extent that two traits have common genetic influences due either to pleiotropy or linkage (Falconer 1981). I estimated the heritability of mating behaviour using two methods (Falconer 1981): parent-midoffspring regression ( N = 34 families) and intra-class correlation based on data from full siblings ( N = 102 brothers). Genetic correlations were estimated from the covariances and cross-covariances of values for father and mean offspring scores for three sons from each father (Falconer 1981).
In pairwise comparisons, offspring of dominant males usually dominated the offspring of subordinate males. In 40 different bouts, offspring of dominant fathers initiated agonistic encounters, exhibited aggressive rather than submissive behaviour and dominated in 34 (85 %) contests. Offspring of subordinate fathers exhibited dominant male behaviour and won only six (15%) contests. These results were significantly different from the null hypothesis of equal probability of exhibiting dominant behaviour (G-test with William's correction, G=21"107, df= 1, P 0'5).
Attractiveness tO mates
Inheritance of Mating Behaviour
For the purposes of the genetic analysis, mating success of accepted and rejected males was considered a non-metric trait with two possible values (success or failure). The heritability of being a rejected male versus being an accepted male was calculated using two methods with different assumptions (Reich et al. 1972; Im & Gianola 1988). The method of Reich et at. (1972) assumes a normally distributed liability underlying the trait. Thus, although the trait has a bimodal expression, it is assumed to have a normal distribution but
There was considerable phenotypic variation in all six courtship behaviours (Table I). There were no significant differences between parent and offspring means and variances after transformation (speed of attraction F=2.723, dr= 1,66; length of post-mating association F = 0.712, dr= 1,66; speed of wing-raise response F = 0.808, dr= 1,66; speed of climb response F = 1.264, dr= 1,66; courtship speed F = 0.803, dr= 1,66; length of copulation F = 2.792, dr= 1,66; all P>0-05). However, the duration of each component of courtship was dependent on the
Mating behaviour
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Table I. Mean duration (SE)of behavioural acts associated with courtship and mating in
N. cinerea Duration in Behaviour Speed of attraction Length of post-mating association Speed of wing-raise response Speed of climb response Courtship speed Length of copulation
Dominant male*
Subordinate male
Pt malet
F~ male
31-47 (5-35) 33.72 (2-89) 3.94 (0.74) 3.61 (0-82) 14.72 (2.73) 703.90 (14.31)
49.23 (7-32) 23.83 (2-95) 6,61 (1.75) 7.61 (1.36) 23,94 (3.07) 660,15 (13.64)
36-83 (3-71) 28-78 (2.70) 5.28 (0.96) 5.61 (0.85) 19.33 (2-17) 682.03 (10.13)
36-11 (3.79) 31-25 (2-58) 5.85 (0.83) 4.73 (1.16) 21.05 (2.24) 715.48 (10.28)
*Comparison of dominant and subordinate male values for each category are all statisticallysignificantlydifferent;ANOVA on log-transformeddata. These data are from the P1 generation, N= 18 for both dominant and subordinate males. tComparison ofP 1(father) and F 1(mean of three male offspring)values for each category are not statistically significantlydifferent; ANOVA on log-transformed data. N = 34 for both F~ and P1. dominance rank of the male (Table l). Dominant males attracted females more quickly ( F = 7-484, dr= 1,34, P
