Multiple paternity increases effective population size

Abstract

The effective size, N e , of a population is generally defined as the size of an ideal population, with constant finite size, no mutation and random union of gametes in each generation, in which the population genetic dynamics are comparable with that of the actual population under study (Wright 1931). An important departure from this ideal is caused by 'clustered reproduction', i.e. the production of multiple offspring by a female in a single reproductive bout (clutch, brood, litter, etc.). In such cases, it is possible that a single male will sire all the offspring in a brood. This combination of clustered reproduction and single paternity (SP) has the potential to reduce a population's N e by increasing the variance in male reproductive success, especially in the case of highly polygynous species (e.g. Storz et al. 2001) or when the variance in female fecundity and offspring survival is high. By contrast, if the father of each offspring in the brood is chosen randomly from the population, then clustered reproduction would have no influence on the variance in male reproductive success. Between these two extremes lies multiple paternity (MP), in which the clustered offspring of a polyandrous female are descended from multiple males, each siring a portion of the clutch. Although in most cases there is still a significant departure from the ideal of random mating, it is generally accepted that MP reduces the variance in male reproductive success and hence increases N e relative to SP in the face of clustered reproduction.In a recent paper, Karl (2008) reviewed the literature on the relationship between MP and N e and concluded that, under most natural conditions, MP does not increase N e relative to SP in an otherwise identical mating system. Karl (2008) admits that this conclusion runs contrary to both theoretical expectations (Sugg & Chesser 1994;Balloux & Lehmann 2003) and the often stated empirical inference (Davis et al. 2001;Shurtliff et al. 2005;Pearse et al. 2006;Moore et al. 2008) but points out that these studies are effectively comparing multiple mating with strict monogamy, which is rare in animals. As multiple mating may also occur in the context of temporal polyandry, in which a female produces several single-sired broods of offspring over its lifetime and may remate between them, Karl (2008) argues that it is more appropriate to compare MP with SP within this context, and that in such a comparison MP will not increase N e .We agree with Karl's (2008) excellent point that MP and temporal polyandry can have similar effects on N e , with temporal polyandry providing an effective equivalent to MP over the lifespan of any female. This similarity has important genetic implications for conservation, yet it is commonly unrecognized in the literature. Notably, studies that detect MP during a single reproductive season, but which do not sample in a manner that allows evaluation of temporal polyandry, do demonstrate an increase in N e relative to SP within broods (Davis et al. 2001;Shurtliff et al. 2005;Pears...

Influence of translocation strategy and mating system on the genetic structure of a newly established population of island ptarmigan

“…Low skew in male reproductive success and high rates of multiple paternity can reduce the impacts of isolation and endemism by functionally increasing N e (Pearse and Anderson 2009). Moreover, at low population densities, such as those that occur at Agattu Island, females may not be able to afford to be choosy until after they have already mated, hence the relatively low skew value we observed.…”

The influence of persistent individual differences and age at maturity on effective population size

“…This has been demonstrated both theoretically [7][8][9][10][11][12] and experimentally [13]. Other factors that affect the variance in reproductive success, and thus N e , are multiple paternity within broods [14], population subdivision [15] and variance in female fecundity [16][17][18]. Nunney [16] examined different types of variation in female fecundity and found that consistent individual effects decreased the effective population size more than random effects or age-related effects.…”

Dispersal and demography of brown trout, Salmo trutta, inferred from population and family structure in unstable Mediterranean streams

“…It is, then, possible that the polygynandry also offset the effect of biased sex ratio, enabling the reproduction of all mature fish during the spawning season. Albeit sometimes questioned, multiple mating is often regarded as a strategy for increasing effective population size (Pearse & Anderson, 2009, and references therein).…”