Reproductive biology

Short life spans, leading in their extreme form to single breeding followed by death in the first year of life (semel-parity), are a defining feature of carnivorous marsupials. Among mammals, semelparity has arisen only in dasyurids and didelphids, in which groups it has evolved at least six times, including in medium-sized species over 2.2 lb (1 kg) in body weight (northern quoll, Dasyurus hallucatus). All carnivorous marsupials, including thylacines and possibly numbats,

A spotted-tailed quoll (Dasyurus maculatus) displays defensive behavior. (Photo by © Erwin & Peggy Bauer. Bruce Coleman, Inc. Reproduced by permission.)

are short-lived, however, compared to similar-sized placental mammals. This entire taxon seems to be evolutionarily disposed towards early senescence.

Semelparity among dasyurids is obligate in most antechi-nuses (Antechinus spp.), in both Phascogale species and in the little red kaluta (Dasykaluta rosamondae), but faculatative in the dibbler and the northern quoll. In the larger antechinuses, complete male die-off occurs immediately after mating but females may live to breed in a second year. The adaptive explanation developed on antechinus to explain die-off postulates that as a consequence of small body size, slow growth and the consequent long period of time required to raise young to independence, and tightly seasonal environments in which food is limiting, males and females are unlikely to be able to gain sufficient energy to breed and then survive to a second year. Their best option may be to put all their energy into one big reproductive effort in the first year, even if it kills them. In antechinuses, a consequence of the need to wean young in a tightly seasonal climate at the time of year when food supplies are maximal is that mating occurs in winter when food resources are scarce. Males are unable to store sufficient fat to see them through the intense mating rut and overcome this energy deficit by using elevated levels of stress hormones to promote the use of protein in muscle tissue as an energy resource. This only becomes possible through complete destruction of the ability to produce more sperm before mating starts (sperm production would interfere with synthesis of stress hormones but also removes any possibility of breeding in a second year) and the shutdown of a negative feedback system that prevents sustained levels of damaging stress hormones in most mammals. Death results from a multitudinous cascade of events related to dramatic loss of body condition and immunosuppression from prolonged elevation of stress hormone levels. Males become anaemic and support huge numbers of ectoparasites, which exacerbates their problems. The proximal cause of death is usually gastrointestinal ulcers or an outbreak of a normally benign disease.

This model is supported by the geographic distribution of semelparous species, which are generally restricted to tightly seasonal environments where reproductive opportunities are limited to a narrow window each year. Iteroparous or multiple-breeding species, such as some dunnarts, include most species from unpredictable arid environments where putting all the eggs in one reproductive basket would be a risky strategy indeed. The lack of sustained elevated stress hormone levels, and opportunities, that come with larger body size and tail fat stores, for sufficient fat storage to tide over the mating period in the northern quoll suggests that a universal model of male die-off remains obscure.

Very small quantities of some of the largest sperm produced by any mammal are other unique features of reproduction in carnivorous marsupials. Complete failure of sperm production prior to the mating period in antechinuses and limited sperm storage leave comparatively small amounts of sperm available for a very intense, once in a lifetime rut; in the brown antechinus (Antechinus stuartii) as few as eight ejaculations. Dasyurid sperm have an unusual form of motility which may compensate for this apparent disadvantage.

Copulation in semelparous species is an intense affair with intromission lasting as long as seven to 12 hours. Given the limited sperm supplies, it must be assumed that sperm is used carefully and ejaculation is timed to maximise the chance of fertilization. Most of the time and energy devoted to mating probably serves the dual functions of stimulating the female and mate guarding, both of which increase the male's chance of siring the young. Physical stimulation provided by the thrusting male during copulation improves sperm transport up the female reproductive tract, and occupying the female in copulo for a substantial proportion of the limited time in which she is in estrus physically prevents other males from mating with her. Antechinus, which mate in communal leks, are able to turn 180° while in copulo and fight off other males. Tasmanian devils indulge in ferocious mate guarding, keeping the female a prisoner in the den for days at a time without food or water, until her estrus is finished or the female's desire to escape reaches such an intensity that she succeeds in fighting off the male. Both male and female are likely to be injured in this process.

The female is by no means a passive spectator in the mating business. Female Tasmanian devils actively assess different males and solicit copulations from the male of their choice, avoiding or fighting off the others. Long periods of behavioral estrus allow time for females to mate with a number of males, resisting mate guarding attempts and fighting each one off in turn.

Multiple paternity has been found in all of the small number of species in which mating systems have been investigated using genetic paternity markers, and suggest high levels of promiscuity among females. Four fathers per litter is not uncommon in devils (four teats) and up to seven fathers have been recorded in the agile antechinus (six to 10 teats), with 50% of litters having three or more. Prolonged copulation, larger than average testes size (correlated with greater sperm production), strong male-biased sexual size dimorphism (males larger than females), intense mate guarding, long periods of behavioral estrus, prolonged periods of sperm storage within the female reproductive tract prior to ovulation, and higher population densities are associated with the likelihood of sperm competition (between the sperm of different males within the female reproductive tract) and possibly the intensity of female choice. Semelparous species such as antechinueses exhibit all of the above traits. Iteroparous species from less predictable, arid environments, such as some dunnarts, do not.

Carnivorous marsupials, at least the dasyurids, have one more trick up their metaphorical sleeves. Together with bats, dasyurids are unique among mammals in having sperm storage facilities in the female reproductive tract. (Sperm storage is common in birds and insects.) Ovulation occurs up to 12 days after behavioral estrus and the sperm of several males are stored, possibly right next to each other, in tiny crypts in the oviducts. The sperm is reactivated and released at ovulation. This puts quite a different spin on how sperm competition might operate.

Parental care in all carnivorous marsupials for which it is known is restricted to maternal care of the young during permanent attachment to the teat and lactation. Once young have permanently vacated the pouch, they are deposited in a vegetation-lined nest in a den (underground burrow, cave, or hollow log). Apart from records of chuditch (western quolls) moving young to new dens on their back, there are no other records of females escorting young outside the den. Juvenile chuditch gradually explore further and further from the mother's den as they grow and teach themselves to forage and hunt. As weaning from lactation approaches, both mother and young start to spend nights apart in different dens. The frequency of these separations increases until the male young disperse. Once the males move away from the mother's home range they move rapidly over long distances.

Among many mammals, and it appears most carnivorous marsupials, it is usually the male offspring that disperse from their mother's home range, females staying close to home for life. Females thus exact a longer term cost to the mother, although the difference in the number of young produced by both good and poor quality females will not be great. If, however, there are major differences among individual males in reproductive success, it may be advantageous for females to invest more heavily in male offspring. Strongly male-biased sex ratios occur in some species of dasyurids, including in agile antechinuses. The mechanism of sperm storage offers possibilities for sex-based sperm selection.

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