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Inbreeding in Littledale's Whistling Rat Parotomys Littledalei

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Inbreeding in Littledale's Whistling Rat Parotomys Littledalei JOURNAL OF EXPERIMENTAL ZOOLOGY 293:171–178 (2002) Inbreeding in Littledale’s Whistling Rat Parotomys littledalei NEVILLE PILLAY Ecophysiological Studies Research Group, School of Animal, Plant and Environmental Sciences, University of the Witwatersrand, WITS 2050, South Africa ABSTRACT Despite its rarity in nature, inbreeding is sometimes evident in species occupying ephemeral, unpredictable habitats, and which occur at low densities. One such species is Littledale’s whistling rat, Parotomys littledalei, a murid rodent endemic to the south-west arid region of South Africa. Using a captive population of P. littledalei, I studied mate choice for kin and nonkin, and the reproductive performance of inbred and outbred pairs. In choice tests, estrous females presented with either odors or actual males showed a preference for siblings or half-siblings to unrelated males. Males did not discriminate between the odor of estrous kin and nonkin. In breeding studies, inbred (mother-son; brother-sister) and outbred (proven female and an unrelated young male and nonsiblings) pairs had a similar reproductive output, although the sex ratio favored males in inbred litters. The development of inbred young was indistinguishable from outbred young. The results indicate that female P. littledalei prefer to inbreed, but there are no apparent advantages to inbreeding over outbreeding. J. Exp. Zool. 293:171–178, 2002. r 2002 Wiley-Liss, Inc. Inbreeding is generally regarded as being disruption of gene complexes (Partridge, ’83; disadvantageous, particularly when mating occurs Shields, ’93). between close relatives, such as between parents Ecologically, inbreeding is apparently more and offspring and siblings (Clutton-Brock and common in populations occupying ephemeral, Harvey, ’76). The detrimental effects of inbreeding patchy, or unpredictable microhabitats than in are well known, and they are assumed to be the those occupying habitats that are permanent and result of increased homozygosity of deleterious predictable (Batzli et al., ’77; Anderson, ’89). In recessive alleles (Charlesworth and Charlesworth, ephemeral-patchy microhabitats, the costs of dis- ’87), affecting, for example, the pre- and post- persal may favor philopatry and mating with kin zygotic viability of inbred offspring (Lacy et al., (Smith and Ivins, ’83; Bollinger et al., ’91), ’96) and the reproductive success of inbred adults particularly at low population densities. For (Margulis, ’98). Many have argued and shown that example, the high level of inbreeding in the the detrimental effects of inbreeding lead to meadow vole Microtus pennsylvanicus may be outbreeding mechanisms through behavioral and explained by the high costs of dispersal between physiological adaptations. widely spaced grassland patches (Pugh and Ta- Despite the wide acceptance of inbreeding marin, ’88). avoidance, it is known that close inbreeding may Littledale’s whistling rat Parotomys littledalei is occur when alternative mates are not available. a medium-sized (adult mass range 107–120 g) For example, mating occurs in sibling groups in murid rodent endemic to the south-west arid some insects upon emergence but females will biome of southern Africa. The known distribution later outbreed (Hamilton, ’93; Chapman and pattern of P. littledalei includes the Nama Karoo, Stewart, ’96). Inbreeding may also occur when the costs of avoiding inbreeding outweigh the Grant sponsor: National Research Foundation; Grant sponsor: benefits (Partridge, ’83; Pugh and Tamarin, ’88; University of the Witwatersrand. Shields, ’93). For example, the costs of dispersing Correspondence to: Neville Pillay, Ecophysiological Studies Re- search Group, School of Animal, Plant and Environmental Sciences, or delaying reproduction may be higher than those University of the Witwatersrand, Private Bag 3, WITS 2050, South of mating with close relatives (Rowley et al., ’86). Africa. E-mail: [email protected] Received 9 November 2001; Accepted 28 February 2002 In addition, inbreeding may maintain adaptations Published online in Wiley InterScience (www.interscience.wiley. to local conditions (Partridge, ’83), and prevent com). DOI: 10.1002/jez.10107 r 2002 WILEY-LISS, INC. 172 N. PILLAY succulent Karoo, the southern Kalahari regions in different sites that were unlikely to be closely the South Africa-Namibia border, and along the related. The F1 offspring were outbred and their Namib and Kunene rivers (Coetzee and Jackson, offspring (F2) were used in experiments. ’99). This distribution covers some of the most Animals were singly maintained in Lab-o-tec arid regions of southern Africa where rainfall may cages (400 Â 250 Â 120 mm) or as pairs in glass be less than 200 mm per annum. aquaria (900 Â 300 Â 400 mm). Environmental The presence of P. littledalei in an area is conditions were partially controlled (22–251C; 30– usually indicated by a complex warren system 70% rH; light regime of 15L:9D, lights on at 0500 under bushes (Coetzee and Jackson, ’99; Jackson, hr). Coarse wood shavings were provided as litter 2000). Apart from providing protective cover and hay was provided as nesting material. Cages against predators and extreme environmental were washed and the shavings were replaced conditions, bushes serve as a source of food; P. weekly. Food was comprised of ad libitum spinach, littledalei is strictly herbivorous, feeding on the vegetable tops (e.g., carrot and beetroot), and Epol leaves of a limited number of succulent and rabbit pellets. Water was provided at all times. nonsucculent vegetation (Coetzee and Jackson, ’99). Field studies indicate that the taxon appar- Mate preference ently does not readily venture beyond the warren to feed or forage (Coetzee and Jackson, ’99), and The preference by individual females and males Jackson (2000) maintains that such burrowing for the odor of related and unrelated opposite sex and foraging habits of P. littledalei effectively individuals was tested in two combinations: (i) restrict its distribution within its geographical littermate sibling vs. unrelated individual; and (ii) range. half-sibling (same father) vs. unrelated individual. Coetzee and Jackson (’99) suggest that locating For each combination, I tested the responses of 15 a suitable bush, a limiting resource in the arid estrous females and 14 males; males were tested environments, will influence dispersal in P. lit- with the bedding of estrous females. The estrous tledalei, and cohabitation has been observed in state of all females (test or stimuli) was deter- large bushes in parts of its distributional range. mined using vaginal smears. Whether such a situation leads to inbreeding in Tests were conducted in a neutral arena, nature is unknown, but I observed inbreeding consisting of a square perspex apparatus (400 Â during an earlier breeding study of captive P. 400 Â 200 mm) connected to three clear, plastic littledalei (Pillay, 2002). Similarly, I showed in two choice chambers (150 Â 150 Â 150 mm) by PVC mesic relatives of P. littledalei that inbreeding is pipes (60 mm internal diameter) at the middle of common in the species (Otomys angoniensis) each side. Each choice chamber contained a petri occupying patchy ephemeral habitats and absent dish (55 mm diameter) with soiled bedding from in the species (O. irroratus) inhabiting dense donor individuals or clean bedding (control). The habitatsFthe latter displaying behavioral in- entrance to each choice chamber was guarded with breeding avoidance (Pillay, ’98). a removable, opaque partition. Prior to each test, The objectives of the present study were to soiled bedding was randomly assigned to one of establish whether male and female P. littledalei the three nest boxes. A test individual was placed discriminate between kin and nonkin in mate in the middle of the test arena. After an acclima- choice tests and to ascertain the reproductive tion period of 10 min, partitions to the choice performance of inbred and outbred pairs. chambers were removed and the time spent within each of the three chambers by test subjects was MATERIALS AND METHODS video-recorded for 15 min under fluorescent lights during the light phase of the light-dark cycleF P. Study animals were live-trapped at Springbok littledalei is a diurnal rodent. After tests, the (291400S, 171530E) in the Northern Cape Province, choice apparatus was thoroughly cleaned with South Africa. Thirty adults were collected from warm soapy water and alcohol, dried, and several sites within the Springbok area. The the floor was covered with a thin layer of wood minimum distance between sites was 400 m, and shavings. although dispersal distances of P. littledalei are Soiled bedding used in choice tests was collected unknown, they are unlikely to exceed 100 m from estrous stimuli females, sealed in air-tight (Jackson, personal communication). In captivity, bags, and stored at À151C until use (after Heth pairings were established between individuals of et al., ’98). It was necessary to freeze samples since INBREEDING IN WHISTLING RATS 173 female P. littledalei do not display synchronous the pair had access to each other and the entire oestrus, making it unlikely that all the appropriate cage. Aggression was minimal or absent at this stimuli were available on one day. For consistency, time, with pairs either nesting together or sepa- bedding from donor males and clean bedding were rately. All females were very aggressive toward also frozen. Frozen samples were thawed out at their mates a week before parturition, so males room temperature just prior to tests. No bedding were removed from the breeding tank at this time was frozen for more than a week. and housed elsewhere. Pairs that had not pro- All test subjects were sexually mature (i.e., 4 duced a litter after 120 days were separated. This 100 days old; Pillay, 2002) virgins that were used time period allowed for 30-day old individuals to once in experiments. None made contact with half- attain sexual maturity (approximately 90 days) siblings or unrelated individuals prior to tests, and and complete gestation (41 days; Pillay, 2002). they were separated from siblings for at least two I compared the reproductive performance of months (i.e., they were housed in different rooms).
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