Mating order and reproductive success in male Columbian ground squirrels (Urocitellus columbianus)

Abstract

Multiple mating by females is common in many mammalian species, often resulting in mixed paternity litters. In such mating systems, mating order, male age, and male body mass frequently play an important role in determining male reproductive success. We tested for these effects on male reproductive success in Columbian ground squirrels (Urocitellus columbianus). The mating activity of estrous females was observed, and the occurrence of sperm precedence was tested using microsatellites to determine paternity in a total of 147 litters (434 offspring), including 110 litters (334 offspring) where the mating position of individual males was determined. Females mated with up to 8 males per litter, whereas paternity analyses revealed that only the first 5 males to mate actually sired offspring. The number of offspring sired significantly decreased with position in the mating sequence, showing a strong first male advantage. The extent of this advantage diminished with an increasing number of male mating partners, indicating that sperm competition plays an important role. A male's position in the females' mating sequences was not consistent within and across seasons, suggesting that individual males did not follow distinct reproductive strategies. Rather, males of intermediate age were more successful than young and old males, when corrected for age effects; heavier males were more likely to mate first. We conclude that males gain the largest part of their seasonal reproductive output from mating first with a female due to a pronounced first male advantage but gain considerable additional fitness from mating with additional, already mated females.

Male reproductive tactics to increase paternity in the polygynandrous Columbian ground squirrel (Urocitellus columbianus)

“…Columbian ground squirrels are colonial, hibernating rodents that inhabit subalpine and alpine meadows of the northern regions of the Rocky Mountains. The active season is short and adult males are typically the first to emerge from hibernation around mid-April, followed by females a few days to a week later (Murie and Harris 1982;Dobson et al 1992;Neuhaus 2000;Neuhaus and Pelletier 2001;Raveh et al 2010).…”

“…Adult males were trapped first, emerging from hibernation in mid-April (average 22.5 April±9.6 SD, range 12 April-26 May, N=71), followed by adult females (29.0 April±6.6, 11 April-17 May, N=154), yearling males (7.4 May±8.9, 16 April-28 May, N=58), and yearling females (8.5 May±8.5, 21 April-30 May, N=90; see also Murie and Harris 1982;Raveh et al 2010). Adult females mated on average 4.4 days after emergence from hibernation (adults 4.4±2.2 SD days, range 3-15, N=134; yearlings 7.0±2.7 days, range 5-11, N=4).…”

“…Hence, males may need to compete for the best position within the mating sequence (e.g., Raveh et al 2010) and adapt their ejaculate size to the intensity of sperm competition (Birkhead and Møller 1998). Or alternatively, males may try to swamp, remove, or block rival sperm (using copulatory plugs, for instance Murie and McLean 1980;Koprowski 1992;Birkhead and Møller 1998).…”

“…These rodent species are especially good models for the study of mating behavior because females exhibit a very brief receptive phase (<12 h) during the breeding season, during which they typically copulate with several males (Hanken and Sherman 1981;Schwagmeyer and Parker 1987;Murie 1995;Lacey et al 1997). Several authors have investigated and reported the existence of sperm precedence in these taxa, including 13-lined ground squirrels, Ictidomys tridecemlineatus (Foltz and Schwagmeyer 1989;Schwagmeyer and Foltz 1990); Belding's ground squirrels, Urocitellus beldingi (Hanken and Sherman 1981;Sherman 1989); in Arctic ground squirrels, Urocitellus parryii (Lacey et al 1997); Idaho ground squirrels, Urocitellus brunneus (Sherman 1989); and Columbian ground squirrels, Urocitellus columbianus (Raveh et al 2010).…”

“…In this study, we investigated copulatory and postcopulatory behaviors in free-living male Columbian ground squirrels (U. columbianus) to identify underlying mechanisms that facilitate first-male sperm precedence and variation in male siring success (see Raveh et al 2010). Previous studies suggested that reproductive male Columbian ground squirrels invest both time and energy in postcopulatory behaviors such as mating calls (Manno et al 2007) and mate guarding (Manno and Dobson 2008).…”