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Cooperative Breeding in Groups of Synchronously Mating Females and Evolution of Large Testes to Avoid Sperm Depletion in African Striped Mice

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Cooperative Breeding in Groups of Synchronously Mating Females and Evolution of Large Testes to Avoid Sperm Depletion in African Striped Mice Schradin, C; Kinahan, A A; Pillay, N (2009). Cooperative breeding in groups of synchronously mating females and evolution of large testes to avoid sperm depletion in african striped mice. Biology of Reproduction, 81(1):111-117. Postprint available at: http://www.zora.uzh.ch University of Zurich Posted at the Zurich Open Repository and Archive, University of Zurich. Zurich Open Repository and Archive http://www.zora.uzh.ch Originally published at: Biology of Reproduction 2009, 81(1):111-117. Winterthurerstr. 190 CH-8057 Zurich http://www.zora.uzh.ch Year: 2009 Cooperative breeding in groups of synchronously mating females and evolution of large testes to avoid sperm depletion in african striped mice Schradin, C; Kinahan, A A; Pillay, N Schradin, C; Kinahan, A A; Pillay, N (2009). Cooperative breeding in groups of synchronously mating females and evolution of large testes to avoid sperm depletion in african striped mice. Biology of Reproduction, 81(1):111-117. Postprint available at: http://www.zora.uzh.ch Posted at the Zurich Open Repository and Archive, University of Zurich. http://www.zora.uzh.ch Originally published at: Biology of Reproduction 2009, 81(1):111-117. Cooperative breeding in groups of synchronously mating females and evolution of large testes to avoid sperm depletion in african striped mice Abstract Testis size has been related to the mating system of both vertebrates and invertebrates. These differences are regarded as adaptive responses to sperm competition in promiscuously mating species. However, not all variation in testis size can be explained by sperm competition. Here, we test the hypothesis that the evolution of large testes occurs when synchronously breeding females must be fertilized within a short period of time to avoid reproductive competition among the females. African striped mouse (Rhabdomys pumilio) males of a polygynous population with cooperative breeding and high risk of sperm depletion had testes and cauda epididymis twice as large as those of males of four different promiscuous populations with high risk of sperm competition. When paired with three females simultaneously in captivity, males of the polygynous population bred with three females within 8 days, leading to synchronous births in their harems, thereby potentially reducing the risk of infanticide. Males from the promiscuous population reproduced with only one or two females within 8 days, and births were not synchronous. We conclude that large testes are selected for in species with synchronously mating females, which is ultimately beneficial for the evolution of cooperative breeding. 1 Cooperative Breeding in Groups of Synchronously Mating Females and 2 evolution of Large Testes to avoid Sperm Depletion 3 4 PUBLISHED AS: 5 Cooperative breeding in groups of synchronously mating females and evolution of large 6 testes to avoid sperm depletion in african striped mice. 7 Schradin C, Kinahan AA, Pillay N. 8 Biol Reprod. 2009 Jul;81(1):111-7. Epub 2009 Mar 4. 9 10 11 Short Title: LARGE TESTES CAN EVOLVE TO AVOID SPERM DEPLETION 12 13 The risk of sperm depletion due to synchronous mating in communally breeding 14 species can lead to the evolution of larger testes 15 16 Keywords: Rhabdomys; sperm competition; communal breeding; reproductive skew 17 18 C. Schradin2,3,4, A. A. Kinahan4, and N. Pillay4 19 20 Zoological Institute 3, University of Zurich, Winterthurerstr. 190, 8057 Zurich, Switzerland. 21 School of Animal, Plant and Environmental Sciences 4, University of the Witwatersrand, 22 Private Bag 3, Wits 2050, Johannesburg, South Africa. 23 2 24 1 Supported by the University of the Witwatersrand (Anderson Capelli Fund), National 25 Research Foundation (grant number: 2069110) and the Swiss National Science Foundation 26 (3100A0-120194). 27 28 2 Correspondence: Carsten Schradin, Zoological 1 Institute, University of Zurich, 29 Winterthurerstr. 190, 8057 Zurich, Switzerland. e-mail: [email protected] 30 31 3 32 ABSTRACT 33 Testis size has been related to the mating system of both vertebrates and invertebrates. 34 These differences are regarded as adaptive responses to sperm competition in 35 promiscuously mating species. However, not all variation in testis size can be explained by 36 sperm competition. Here we test the hypothesis that the evolution of large testes occurs 37 when synchronously breeding females have to be fertilized within a short time period to 38 avoid reproductive competition among the females. African striped mouse (Rhabdomys 39 pumilio) males of a polygynous population with cooperative breeding and high risk of 40 sperm depletion had twice as large testes and cauda epididymis than males of four different 41 promiscuous populations with high risk of sperm competition. When paired with three 42 females simultaneously in captivity, males of the polygynous population bred with three 43 females within 8 days, leading to synchronous births in their harems, thereby potentially 44 reducing the risk of infanticide. Males from the promiscuous population reproduced with 45 only one or two females within 8 days and births were not synchronous. We conclude that 46 large testes are selected for in species with synchronously mating females, which is 47 ultimately beneficial for the evolution of cooperative breeding. 48 49 50 INTRODUCTION 51 When females mate with more than one male simultaneously, the potential for sperm 52 competition arises [1]. As a result, promiscuous species such as the chimpanzee have much 53 larger testes than monogamous or polygynous species where a single male mates with one 54 or with several females successively, such as the gorilla [2-4]. Males of the promiscuous 55 wild guinea pig Galea musteloides have much larger testes than males of the polygynous 4 56 wild guinea pig Cavia aperea [5-7]. Dung flies (Scathophaga stercorcaria) kept under 57 polyandrous circumstances for 10 generations evolved much larger testes than those kept 58 monogamously [8]. Many studies demonstrate correlations between testis size and 59 correlates of sperm competition, such as group size and mating system [3, 8-15], and show 60 that males with larger testes sire more offspring under conditions of sperm competition 61 [16]. In addition, in several rodent species, males can adjust the size of their ejaculates 62 depending on the risk of sperm competition, e.g. as a consequence of perceived olfactory 63 cues from other males [17, 18]. 64 There is large variation in testis size among species, which can be explained to 65 some extent by sperm competition, but significant variation remains unexplained [3, 19, 66 20]. In addition to sperm competition, testis size might be influenced by sperm depletion. 67 The sperm depletion hypothesis proposes that males of taxa that copulate often have 68 relatively larger testes [21, 22]. Males must trade-off between costly sperm production and 69 investment in other life history traits such as parental care [10] or energy invested into mate 70 searching. In mammals (but not in all other taxa, [23]), the sperm production rate per gram 71 parenchyma is constant, i.e. independent of testis size, such that larger testes produce more 72 sperm and can provide a larger sperm reserve in the cauda epididymis [19, 24]. Thus, 73 within a single species, males with larger testes can produce more sperm, giving them an 74 advantage under conditions of sperm competition [24]. Additionally, males with larger 75 testes can also ejaculate more often, i.e. theoretically, they can copulate with and 76 inseminate more females, as they are less likely to experience sperm depletion [16]. 77 Here we compare testis size between males of a single species that experience either 78 a high degree of sperm competition or are at a high risk of sperm depletion. Striped mice 79 (Rhabdomys pumilio; adult body mass 30-80g, diurnal, [25]) show high intra-specific 5 80 variation in their mating systems [26, 27]. In moist grasslands, characterized by a 6 month 81 long breeding season and low population density, striped mice live solitarily [27]. Females 82 defend territories against other females while males follow a roaming tactic, having home 83 ranges twice as large as those of females. Male home ranges overlap with the territories of 84 several females, and the territory of each female overlaps with several males. Males and 85 females only associate for mating and females can mate with several males, leading to a 86 high risk of sperm competition [27-29]. Females from these grassland populations display 87 synchronous estrus in captivity [30], and there is some indication of reproductive 88 synchrony in nature [31]. In contrast, striped mice show a system of harem defense 89 polygyny in the semi-desert Succulent Karroo, characterized by a short 3 month breeding 90 season and high population density [25]. Groups of up to 4 closely related, cooperatively 91 breeding females (as indicated by genetic studies; Schradin & Lindholm, unpubl. data) are 92 defended by a single territorial breeding male [32, 33]. Males and females of one group 93 share one territory and have home ranges of similar size [27, 33]. In contrast to the roaming 94 males from the grasslands, semi-desert males invest in territory defense [32, 33], in 95 particular by patrolling their territory boundaries [34] and aggressively repelling male 96 intruders [32]. Thus, males of this polygynous population are thought to experience lower 97 levels of sperm competition. The females in their harems breed synchronously [33], i.e. 98 males must be able
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