E. A Male Reproductive Postponement State

The reproductive postponement state of males is similar to that of females. It is mediated by activity of an "anti-gonad system" that usually includes activity of the pituitary-adrenal axis and their hormones ACTH and adrenal corticosteroids. It is stimulated during climatic and social adversity, as in the female, with the latter mediated by ACTH secretion as a motor pattern of prolonged defense and submission. The male's reproductive physiology and sexual activity is turned off, due to the suppression of gonadotropins and gonadal hormones And there are a variety of effects upon the motivational systems of social behavior.

As in the female, the ACTH and adrenal corticosteroids act directly upon some motivational systems to suppress fighting behavior. At brain site 1, the male's offense motivational mechanism is suppressed by ACTH, and at brain site 6, his consociate modulator is facilitated by corticosteroids. The suppression of androgen production also greatly limits the male's social behaviors. Exploration and marking, dependent upon androgen, is no longer activated (brain site 2). Offense against conspecific males, dependent upon an androgen-activated olfactory filter, no longer receives its critical motivating stimuli (brain site 7). The size of pheromone-secreting glands is diminished as is the production of various androgen-dependent pheromones.

The advantage of a reproductive postponement state for a male is less obvious than for a female. For a female, it enables her to avoid the great risks associated. With the female role in reproduction. For the male, on the other hand, the risks are not so obvious. It is true territorial maintenance and fighting do require energy expenditure and a certain vulnerability to predators and opposition males, but in a stable system of "loyal opposition" these may be minimized. And the actual metabolic cost of the production of sperm and the reproductive act itself are quite small.

In those species with seasonal reproductive cycles for the females, the males also show similar seasonal cyclicity. In this case the advantage is not difficult to understand; after all, if the females are not receptive, there is little advantage gained for males by maintaina reproductive state. For example, Turner and Iverson (1973) have recorded seasonal cycles of aggressiveness in :Microtus pennsylvanicus and compared it to the seasonal cycle of spermatogenesis that "begins when circulating levels of testosterone increase." Healey (1967) recorded a similar seasonal cycle in aggressiveness in Peromyscus maniculatus, found that it was correlated with average testes size, and concluded that "in deermice the whole cycle in aggressiveness is probably related to sexual maturity and testosterone levels." Although seasonal cycles have been observed in both aggressiveness and breeding in outdoor colonies of Rattus norvegicus (Calhoun, 1962a), there are no experimental studies on this or other laboratory species on the role of hormones in seasonal changes of offense.

Perhaps as a result of reduced androgen levels, large groups of muroid rodents may often be found together in common burrow systems or nests during the non-breeding season. This is the case in certain gerbils, voles, and mice (Naumov, 1972), Apodemus, (Zimmerman, 1952), Micromys (Frank, 1957), Oryzomys (Negus et a1, 1961), Ondatra (Steiniger, 1976), and Peromyscus (Metzgar, 1971). Presumably, the animals gain some advantage from the conservation of heat during the winter in such assemblages. In fact, there are few reports of muroid rodents in temperate climates that do maintain individual territories throughout the year, most of the reports pertaining to species of the genus Microtus (Turner and Iverson, 1973; Rose and Gaines, 1976; Krebs et a1, 1973; Getz, 1961). This peculiarity of certain microtine rodents correlates with their unusual characteristic of year-round reproduction,

The male reproductive postponement state characterizes the "subordinate" males that have been defeated in territorial contests and the "pathological" populations of males that have been described in conditions of overcrowding. These phenomena have been documented in many studies and frequently reviewed {Christian, 1971, 1975; Christian and Davis, 1964; Archer, 1970; Brain, 1971,1972). The subordinate males are characterized by high resting levels of corticosteroids and greater than normal corticosteroid responsiveness to motivating stimuli of defense or administration of ACTH (E1y and Henry, 1978). In addition to lower levels of offense behavior, subordinate males of various muroid rodent specie s are regularly found to have lower levels of exploration/marking, including locomotion (Mackintosh, 1970), urine marking (Desjardins et a1, 1973; Maruniak et a1, 1974), facial-anointing (Thiessen et aI, 1976), and ventral-rub (Nyby et aI, 1970; Thiessen et aI, 1970a; Gallup and Waite, 1970). In addition, subordinate animals have reduced preputial glands (Davis and Christian, 1957; Bronson and Marsden, 1973) and flank glands (Drickamer and Vandenbergh, 1973; Drickamer et aI, 1973).

The most important advantage derived by a defeated male, or a male under conditions of overcrowding, from a reproductive postponement state may come from the fact that his androgen-dependent pheromone production is curtailed and his scent-marking behavior is suppressed (Leshner, 1975). Under the best of conditions these pheromones enable him to attract females, stimulate their reproductive behavior, and stimulate their hormonal changes necessary for successful reproduction. At the same time, however, these pheromones provide the critical motivating stimuli for the offensive attack of competitive males, and they may serve as attractants for predators. The male cannot have it both ways; either he can attract and mate with females, in which case he must also attract and provoke the attack of competing males and perhaps attract predators as well; or he can reduce his attackability by ceasing to produce and broadcast androgen-dependent pheromones, in which case he also reduces his reproductive potential.

There is a big difference, from the point of view of the behavior of. the population as a whole, between reproductive postponement caused by seasonal factors and reproductive postponement caused by overcrowding and defeat. In the former, there is synchrony among all males and females. In the latter, there is usually a pronounced asynchrony. population divides into "haves" and "have-nots" with some males intensifying their reproductive readiness state and territoriality, while other males shift completely to a reproductive postponement state and become subordinates. In the former case the synchrony is caused by the universal quality of the climatic and biological clock stimuli trigger an "anti-gonad system." In the latter, the asynchrony is caused by the non-universal occurrence of defeat, that activates the defense motivational system and the motor patterns of ACTH secretion, etc. Some animals win and become tyrants; other lose and become pariahs. The documentation for such behavioral dynamics in overcrowded populations is enormous and will not be reviewed here.

There is good documentation for the advantage to be gained by maintaining a successful reproductive readiness state during overcrowding, but there is little documentation for the advantage of a reproductive postponement state. The reason for this may come from the salience of the former animals to the observer of population dynamics, and the difficulty of making the long-term detailed study of both population dynamics and individual life histories which is necessary to document the latter. Thus Calhoun (1962a) observed a great natural selective advantage for the dominant animal in his pen of wild rats. Of 132 infants born and raised in the final year of his experiment (1949),92 were from three sub-colonies containing only 8 of the 61 adult males in the pen, of which three were the most dominant males in the pen. Similar results have been documented with marker genes by DeFries and McClearn (1970) in mice. The best evidence for effectiveness of' a reproductive postponement state derives from a study on a non-muroid rodent, the arctic ground squirrel, by Carl (1971). Over a period of two seasons, approximately half of the adult males obtained territories and the other half remained as "floaters," subordinate males who apparently were in a reproductive postponement state. Of these 22 floater males, 5 were able to obtain territories later, upon the disappearance of the formerly territorial males.

Why is there such a sharp dichotomy between reproductive and reproductive postponement states? Why should they be mediated by mutually inhibitory hormonal systems, gonad and anti-gonad, which leave little room for intermediate strategies.? As mentioned before, a male cannot have it both ways; either he can attract females in which case he invites attack by other males, or else he forfeits his at tractability to females in return for a reduction in his attackability by other males. Under these conditions an especially important factor may be the female's role in the initiation of courtship, a role that has been insufficiently studied (McClintock and Adler, 1978). It is likely that the female is differentially attracted to males with sufficient androgen to produce androgen-dependent pheromones (see brain site 9), a strategy that should prove successful over many generations because it would provide an especially effective genotype for the male offspring. In a population that is partitioned into territory holders and surplus males, dominants and subordinate males in a reproductive state and other males in a reproductive postponement state, it is to her advantage to choose the former animals and avoid the latter. In so doing, she will provide her male offspring with a genotype more likely to make him a dominant, territorial animal with an effective reproductive strategy. Given a population with many such "choosy" females, a defeated male will find little advantage from such an intermediate social strategy, and he might as well adopt a fully-developed reproductive postponement state.

As mentioned earlier, one type of reproductive postponement state combines aspects of both seasonal factors and overcrowding. It is not uncommon in many species for juveniles born late in the season to postpone the usual date of gonadal maturity until the following spring. This would be particularly advantageous in years of high population density, and in populations in which strict territoriality is relaxed during the winter. Animals that postponed their maturity would not have to fight for a territory until they had grown to a large size the spring, at which time they might have a better chance to win in aggressive encounters.

References A-B

References C-H

References J-P

References Q-Z

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