Paternity and male mating strategies of a ground squirrel ( Ictidomys parvidens ) with an extended mating season

Abstract

Animal mating systems are driven by the temporal and spatial distribution of sexually receptive females. In mammals, ground-dwelling squirrels represent an ideal clade for testing predictions regarding the effects of these parameters on male reproductive strategies. While the majority of ground squirrel species have a short, highly synchronous annual breeding season that occurs immediately after females emerge from hibernation, the Mexican or Rio Grande ground squirrel ( Ictidomys parvidens ) differs markedly in having an extended mating season (2 months) and a long delay between emergence from hibernation and female receptivity (1–2 months). Both traits are expected to favor polygyny by increasing the chances that a male can secure matings with multiple females (e.g., females that come into estrus on different days). To test this prediction, we used microsatellite markers to characterize the mating system of a population of Rio Grande ground squirrels from Carlsbad, New Mexico. Our analyses indicated a high frequency of multiple paternity of litters in this population. Paternity was not related to spatial overlap between known mothers and assigned fathers, suggesting that territory defense is unlikely to be an effective male reproductive strategy in the study population. Dominance interactions among males were frequent, with heavier males typically winning dyadic interactions. Surprisingly, however, males with lower dominance scores appeared to have higher reproductive success, as did males that were active over a greater extent of the study site. Collectively, these results suggest that the mating system of the Rio Grande ground squirrel is best described as scramble competition polygyny, with the primary male reproductive strategy consisting of searching for estrous females. Similar patterns of male–male competition have been reported for a few other ground squirrel species, providing potentially important opportunities for comparative studies of the factors favoring this form of male reproductive strategy.

Intraspecific variation in male mating strategies in an African ground squirrel (Xerus inauris)

“…These highly synchronous breeding seasons result in multiple receptive females in a single day, such that males often leave to search and compete for additional females after the initial mating bout to gain greater reproductive advantages (Lacey & Wieczorek, 2001 ; Raveh et al, 2010 ; Sherman, 1989 ). Elongating the breeding season or distance between receptive females affects the costs and benefits of acquiring partners and alters which mating strategies are most successful (Brashares & Arcese, 2002 ; Schwanz et al, 2016 ; Shuster & Wade, 2003 ). X. inauris differ from other sciurids as they are not constrained by winters and can breed year‐round (Waterman, 1996 ).…”

“…The spatial and temporal distribution and density of receptive females impact competition dynamics by altering the costs and benefits of acquiring partners and ultimately influence male reproductive decisions and physiology (Brashares & Arcese, 2002 ; Emlen & Oring, 1977 ; He et al, 2019 ; Schradin et al, 2010 ; Shuster & Wade, 2003 ). In species lacking male parental care, male reproductive success is generally limited by the number of acquired mates, such that males balance current and future reproductive opportunities depending on whether females are economically defendable in space and time (Clutton‐Brock, 1989 ;Emlen & Oring, 1977 ; Schwanz et al, 2016 ). When females are dispersed or when reproduction is asynchronous, traits that enhance male mate searching abilities and dominance hierarchies will be favored (Emlen & Oring, 1977 ; Schwanz et al, 2016 ).…”

“…In species lacking male parental care, male reproductive success is generally limited by the number of acquired mates, such that males balance current and future reproductive opportunities depending on whether females are economically defendable in space and time (Clutton‐Brock, 1989 ;Emlen & Oring, 1977 ; Schwanz et al, 2016 ). When females are dispersed or when reproduction is asynchronous, traits that enhance male mate searching abilities and dominance hierarchies will be favored (Emlen & Oring, 1977 ; Schwanz et al, 2016 ). Alternatively, females clumped together with discrete breeding seasons favor traits that aid males in direct competition or monopolization (Lacey & Wieczorek, 2001 ; Waterman, 2007 ).…”

“…Ground‐dwelling sciurids represent a continuum of social organization and mating systems, making them an ideal clade to explore variation in male reproductive strategies (Schwanz et al, 2016 ). The Cape ground squirrel ( Xerus inauris ) lies at one end of that spectrum with extreme promiscuity and sociality (Figure 1 ).…”

Polyandry and Polygyny in a Social Rodent: An Integrative Perspective Based on Social Organization, Copulations, and Genetics

“…Previous studies documenting both behavioral and genetic polyandry and polygyny for a diverse array of other animals typically have involved smaller sample sizes over a shorter time span (Hanken and Sherman, 1981;Burke et al, 1989;Moore and Ball, 2002;Solomon et al, 2004). Some previous researchers have used the term "polygynandry" to describe a species in which behavioral and genetic estimates of polyandry and polygyny are both high (Davies, 1992;Baker et al, 2004;Dugdale et al, 2007;Munroe and Koprowski, 2011;Raveh et al, 2011;Schwanz et al, 2016). Perhaps polygynandry is also a good term to describe WTPDs, for which females commonly are both monandrous and polyandrous (behaviorally and genetically) and males commonly are both monogynous and polygynous (behaviorally and genetically).…”