Multiple paternity and sporophytic inbreeding depression in a dioicous moss species

Abstract

Multiple paternity (polyandry) frequently occurs in flowering plants and animals and is assumed to have an important function in the evolution of reproductive traits. Polyandry in bryophytes may occur among multiple sporophytes of a female gametophyte; however, its occurrence and extent is unknown. In this study we investigate the occurrence and extent of multiple paternity, spatial genetic structure, and sporophytic inbreeding depression in natural populations of a dioicous bryophyte species, Sphagnum lescurii, using microsatellite markers. Multiple paternity is prevalent among sporophytes of a female gametophyte and male genotypes exhibit significant skew in paternity. Despite significant spatial genetic structure in the population, suggesting frequent inbreeding, the number of inbred and outbred sporophytes was balanced, resulting in an average fixation coefficient and population level selfing rate of zero. In line with the prediction of sporophytic inbreeding depression sporophyte size was significantly correlated with the level of heterozygosity. Furthermore, female gametophytes preferentially supported sporophytes with higher heterozygosity. These results indicate that polyandry provides the opportunity for postfertilization selection in bryophytes having short fertilization distances and spatially structured populations facilitating inbreeding. Preferential maternal support of the more heterozygous sporophytes suggests active inbreeding avoidance that may have significant implications for mating system evolution in bryophytes.

Balance between inbreeding and outcrossing in a nannandrous species, the moss Homalothecium lutescens

“…Sporophyte production has been shown to be resource limited and abortion of sporophytes in an early developmental stage is not uncommon (Hughes, 1979;Stark and Stephenson, 1983;Stark et al, 2000;Ehrlén et al, 2000). A recent study of Sphagnum lescurii showed that females preferentially supported sporophytes with higher heterozygosity in populations with significant spatial genetic structure (Szövényi et al, 2009). If postfertilization selection based on sporophyte heterozygosity occurs in a moss with dwarf males, the level of heterozygosity in the sporophytes would be higher than what is expected from the available male sexual partners (that is, dwarf males on or nearby the mother shoot).…”

“…The life stage that is most likely to suffer from inbreeding depression is the diploid sporophytic phase . The studies that have attempted to address the relationship between heterozygosity and fitness in sporophytes of various bryophyte species have rendered conflicting results, suggesting that inbreeding depression may be present under certain circumstances but not others Szövényi et al, 2009;Perroud et al, 2011;Jesson et al, 2012;McDaniel and Perroud, 2012;Johnson and Shaw 2015). If the level and risk of inbreeding depression varies greatly between different populations, the selection pressure to avoid inbreeding is also expected to differ.…”

“…The spatial separation of the (often numerous) branches from which the perichaetia are produced (F Rosengren, personal observation) likely reduces the chance of a single male fertilizing all archegonia. Frequent polyandry has previously been reported for S. lescurii, where on average 64% of the sporophytes on each female shoot had been sired by distinct fathers (Szövényi et al, 2009). Mating with multiple males is a prerequisite for the possibility of post-fertilization selection and could thus be essential in populations where such mechanisms have developed (for example, to prevent inbreeding).…”

“…No evidence of post-fertilization selection Because of the fact that bryophytes have limited possibility to assess mate quality before fertilization (Szövényi et al, 2009), postfertilization selection could potentially be an efficient way of increasing the fitness of the sporophytes. However, we found no evidence of post-fertilization selection favouring more heterozygous sporophytes in the sexual reproduction.…”

“…When the distinct fathers each sire an equal number of sporophytes on a female shoot, the effective number of fathers (K E ) will be the same as the number of distinct fathers (K). To get a general estimate of the level of paternity skew, we calculated the mean value of K E /K over all female shoots (Szövényi et al, 2009); this index ranges between 0 (high paternity skew) and 1 (no paternity skew).…”