Reproductive suppression

Reproductive suppression is the prevention or inhibition of reproduction in otherwise healthy adult individuals. It occurs in birds, mammals, and social insects. It is sometimes accompanied by cooperative breeding. It is maintained by behavioral mechanisms such as aggression, and physiological mechanisms such as pheromone signalling. In evolutionary terms, it may be explained by the theory of inclusive fitness.

Overview

Reproductive suppression is the prevention or inhibition of reproduction in otherwise healthy adult individuals. It includes delayed sexual maturation (puberty) or inhibition of sexual receptivity, facultatively increased interbirth interval through delayed or inhibited ovulation or spontaneous or induced abortion, abandonment of immature and dependent offspring, mate guarding, selective destruction and worker policing of eggs in some eusocial insects or cooperatively breeding birds, and infanticide of the offspring of subordinate females either by directly killing by dominant females or males in mammals or indirectly through the withholding of assistance with infant care in marmosets and some carnivores. The reproductive suppression model holds that "females can optimize their lifetime reproductive success by suppressing reproduction when future (physical or social) conditions for the survival of offspring are likely to be greatly improved over present ones”. When intragroup competition is high it may be beneficial to suppress the reproduction of others, and for subordinate females to suppress their own reproduction until a later time when social competition is reduced. This leads to reproductive skew within a social group, with some individuals having more offspring than others. The cost of reproductive suppression to the individual is lowest at the earliest stages of a reproductive event and reproductive suppression is often easiest to induce at the pre-ovulatory or earliest stages of pregnancy in mammals, and greatest after a birth. Therefore, neuroendocrine cues for assessing reproductive success should evolve to be reliable at early stages in the ovulatory cycle. Reproductive suppression occurs in its most extreme form in eusocial insects such as termites, paper wasps and honeybees, and in a mammal, the naked mole rat, which depend on a complex division of labor within the group for survival and in which specific genes, epigenetics and other factors determine whether individuals will permanently be unable to breed or able to reach reproductive maturity under particular social conditions. It is found, too, among cooperatively breeding fish; cooperatively breeding birds such as some woodpeckers; and mammals in which a breeding pair depends on helpers whose reproduction is suppressed. In eusocial and cooperatively breeding animals, most non-reproducing helpers engage in kin selection, enhancing their own inclusive fitness by ensuring the survival of offspring they are closely related to. Wolf packs suppress subordinate breeding.

Pre-fertilization

Environmental cues

Food shortage Female mammals experience delays in the onset of puberty or increase their interbirth intervals in response to environmental conditions that are associated with low abundance and poor quality of foods. Nutritional stress is apparently linked to the female endocrine system and ovulatory pheromonal cycle. For example, Orangutans (Pongo pygmaeus) experience high ketone (due to fat burning) and low estrogen levels during times of low food availability and poor food quality, but low ketone and high estrogen levels that stimulates onset of the ovulation during the fruit masting seasons that occurs about every four years on Sumatra. Since adult female orangutans are solitary, interference by other females can be ruled out as influencing their temporary reproductive suppression and facultatively long interbirth intervals. Polygynandrous yellow baboons (Papio cynocephalus) in Kenya were far less likely to ovulate or conceive during periods of drought or extreme heat, especially if they live in large groups, resulting in longer interbirth intervals during periods of nutritional and thermal stress.

Population density

High population density can lead to reproductive suppression. For example, when high numbers of yellow baboon (Papio cynocephalus) females are simultaneously in estrous at Mikumi National Park, Tanzania, dominant females form coalitions that attack subordinate females, disrupting their reproductive cycle and preventing conception. This places constraints on the number of offspring born in a single generation. Since infant mortality in these baboons depends in part on the number and ages of other infants born into the group, pre-ovulatory females that are most susceptible to stress-induced delay or inhibition of ovulation are the most frequent targets of female coalition attacks. Female attackers are often in advanced stages of pregnancy and have the most to lose if the number of infants in the group reaches an unsustainable level. A similar study of Chacma baboons (Papio ursinus) noted high levels of female-female aggression around the mating season when the number of ovulating females was high (indicated by sexual swellings) and that aggression directed toward suppressing the mating opportunities of ovulating females. Among elephant seals (Mirounga), high neonatal mortality occurs when the number of pups born in a season is high, with deaths resulting from injury and starvation. To counteract loss of their pups elephant seals conceive next year's offspring immediately after giving birth to this year's young, but delay implantation for 4 months. Female striped mice (Rhabdomys pumilio) in monogamous social groups do not experience reproductive suppression, but those living in communally breeding groups with high population density and large numbers of old breeding females do.

Social cues

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