Females Choose Mates Based on Genetic Relatedness in a Small Dasyurid Marsupial, the Agile Antechinus (Antechinus agilis)

Abstract

Females in a variety of taxa mate with more than one male during a single oestrus and exhibit mate preferences for genetically compatible males, but the influence of female mate choice on siring success is not clearly understood. Whether females choose to mate with more than one male or endure forced copulations is also often unknown. Here, we examined the effects of genetic relatedness on female mate choice and siring success in a small semelparous carnivorous marsupial, the agile antechinus (Antechinus agilis), during two consecutive breeding seasons. Experimental trials were conducted in captivity over periods of 72 hours using interconnected enclosures in which female antechinus could choose to access any of four separated males, but males were only able to access females that entered their quarters. Females had access to two genetically similar and two genetically dissimilar males simultaneously and all behavioural interactions were observed and scored from continuous video recordings. Genetic similarity between mates and paternity of young was determined by microsatellite analyses. Some females chose to enter and mate with more than one male during a single oestrus period. Although females investigated all males, they spent significantly more time visiting, and mated more times with, genetically dissimilar males. Males that were genetically dissimilar to the female sired 88% of subsequent offspring. Whilst males mated readily with most females, they rejected the advances of some receptive females, indicating a previously unexpected level of male mate choice. The results show that genetic relatedness between mates has a significant influence on mate choice, breeding and siring success in the agile antechinus.

Fig 1. Enclosures for female choice experiments.

(a) Enclosure seen from above, showing the four male and one female compartments and furnishings. Four outer compartments, with external measurements 400 mm × 300 mm × 300 mm high, each housed a single male and the middle compartment, measuring 800 mm × 200 mm × 300 mm, housed two females. Each male compartment contained a stainless steel nest-box (130 mm × 130 mm × 130 mm) filled with cotton bedding, a cardboard tube, water bowl, feed tray and plastic climbing lattice on one wall. The female compartment contained a nest-tube with cotton bedding (200 mm long × 100 mm diameter) which had entrance/exit holes at each end, plus a water bowl, feed tray and lattice placed at each end. Holes (3 mm diameter) were drilled every 30 mm around the base and top of the four outer walls of the enclosures to allow air flow and in two lines near the base of the walls between the male and female compartments to facilitate movement of animal scents. In the centre of the wall separating each male compartment from the female compartment, a 70 mm × 70 mm gap was covered by a removable clear perspex ‘door’ which contained a 15 mm diameter hole. The size of the hole allowed the exclusion of the larger males which were unable to leave their own compartment in this sexually dimorphic species and allowed almost all females to move in and out of the male and female compartments uninhibited. Females were able to see and interact with males through the perspex and hole. Doors were recessed into a groove across the centre of a wooden ‘door step’ (60 mm × 70 mm × 20 mm high) with grooves on either side of the door to provide grip. (b) Video surveillance set-up showing the enclosure, video camera and video recorder.

Fig 2. The number of visits and time spent at male doors.

The mean (± SE) number of times female agile antechinus (n = 28) visited the doors of males that were more genetically similar and more dissimilar to themselves (left) and the mean (± SE) time (seconds) female agile antechinus (n = 28) spent visiting the doors of males that were more genetically similar and more dissimilar to themselves (right). An asterisk (*) indicates a significant difference from the other value (p = 0.003).

Fig 3. The number of entries and time spent in male enclosures.

The mean (± SE) number of times female agile antechinus (n = 28) entered into the compartments of males that were more genetically similar and more dissimilar to themselves (left) and the mean (± SE) time (hours) female agile antechinus (n = 21) spent in the compartments of males that were more genetically similar and more dissimilar to themselves (right). An asterisk (*) indicates a significant difference from the other value (p = 0.046).

Fig 4. The number females that mated with genetically similar and dissimilar males and paternity of young produced.

The mean (± SE) number of females that mated with the more genetically similar and more dissimilar males (left), and the number of agile antechinus young sired by the more genetically similar and more dissimilar males. Asterisks (*) indicate significant differences in pairs of values (number of matings, p <0.001; number of young, p < 0.016).