Context-dependent autonomous self-fertilization yields reproductive assurance and mixed mating

Abstract

The evolution of self-fertilization in hermaphrodites is opposed by costs that decrease the value of self progeny relative to that of outcross progeny. However, self-fertilization is common in plants; 20% are highly selfing and 33% are intermediate between selfing and outcrossing. Darwin proposed an adaptive benefit of self-pollination in providing reproductive assurance when outcrossing is impossible. Moreover, if outcross pollen receipt is inconsistent within or between years, these conditions likewise favour self-pollination, and this can result in a mixture of self and outcross seed production (mixed mating). Despite wide acceptance, the reproductive assurance hypothesis has lacked the support of complete empirical evidence to show that variable pollination can create both the ecological and genetic conditions favouring self-pollination. We recently showed in Collinsia verna that during periods of infrequent pollinator visits, autonomous self-pollination boosted seed output per flower, the key ecological condition. Here we show low inbreeding depression and marker-based estimates of selfing, demonstrating that when the pollination environment in wild populations necessitates reproductive assurance, selfing rates increase. We provide a complete demonstration of reproductive assurance under variable pollination environments and mechanistically link reproductive assurance to intermediate selfing rates through mixed mating.

Mixed Mating in Homostylous Species: Genetic and Experimental Evidence from an Alpine Plant with Variable Herkogamy,Primula halleri

“…Importantly, herkogamy is known to decrease during anthesis in some species, potentially increasing opportunity for autonomous selfing in later stages of anthesis (Luijten et al 1999;Armbruster et al 2002;Duan et al 2010;de Vos et al 2012). Such delayed selfing represents a mechanism whereby selfing can provide reproductive assurance without interfering with outcrossing opportunities in early anthesis (Lloyd 1992;Lloyd and Schoen 1992;Kalisz et al 1999Kalisz et al , 2004Eckert et al 2006) Thus, delayed selfing enables the benefits of selfing via increasing total reproductive output, without incurring the discounting costs associated with using gametes for selfing that could have been otherwise outcrossed (Herlihy and Eckert 2002). Delayed selfing was proposed to always be favored by selection (Lloyd 1992), offering an explanation for mixed mating as a best-ofboth-worlds solution to the problem of unreliable pollinator service (Kalisz et al 2004;Morgan and Wilson 2005).…”

“…Such delayed selfing represents a mechanism whereby selfing can provide reproductive assurance without interfering with outcrossing opportunities in early anthesis (Lloyd 1992;Lloyd and Schoen 1992;Kalisz et al 1999Kalisz et al , 2004Eckert et al 2006) Thus, delayed selfing enables the benefits of selfing via increasing total reproductive output, without incurring the discounting costs associated with using gametes for selfing that could have been otherwise outcrossed (Herlihy and Eckert 2002). Delayed selfing was proposed to always be favored by selection (Lloyd 1992), offering an explanation for mixed mating as a best-ofboth-worlds solution to the problem of unreliable pollinator service (Kalisz et al 2004;Morgan and Wilson 2005). However, the mating system consequences of decreasing herkogamy during anthesis may be complex, as they can lead to particularly variable selfing rates (Pérez et al 2013), and they remain generally poorly documented.…”

O father where art thou? Paternity analyses in a natural population of the haploid–diploid seaweed Chondrus crispus

“…Once the deleterious mutations have been purged from the population by selection, there will no longer be a cost to selfing and it can become adaptive. For example, if a species is limited in their opportunities to breed by seasonality, pollen limitation, low densities or short lifespans, selfing can be a form of reproductive assurance (Hardy et al, 2004;Kalisz et al, 2004).…”

The mixed mating system of the sea palm kelpPostelsia palmaeformis: few costs to selfing

“…However, individuals will sometimes self regardless of detrimental phenotypic effects [9][10][11]: an evolutionary trade-off described by the reproductive assurance hypothesis [12,13]. When species are limited in their opportunities to breed by seasonality or short lifespan, selfing can be a form of reproductive assurance [14,15].…”