Evolution of seed mass associated with mating systems in multiple plant families

Abstract

In flowering plants, the evolution of self‐fertilization (selfing) from obligate outcrossing is regarded as one of the most prevalent evolutionary transitions. The evolution of selfing is often accompanied by various changes in genomic, physiological and morphological properties. In particular, a set of reproductive traits observed typically in selfing species is called the “selfing syndrome”. A mathematical model based on the kinship theory of genetic imprinting predicted that seed mass should become smaller in selfing species compared with outcrossing congeners, as a consequence of the reduced conflict between maternally and paternally derived alleles in selfing plants. Here, we test this prediction by examining the association between mating system and seed mass across a wide range of taxa (642 species), considering potential confounding factors: phylogenetic relationships and growth form. We focused on three plant families—Solanaceae, Brassicaceae and Asteraceae—where information on mating systems is abundant, and the analysis was performed for each family separately. When phylogenetic relationships were controlled, we consistently observed that selfers (represented by self‐compatible species) tended to have a smaller seed mass compared with outcrossers (represented by self‐incompatible species) in these families. In summary, our analysis suggests that small seeds should also be considered a hallmark of the selfing syndrome, although we note that mating systems have relatively small effects on seed mass variation.

The selfing syndrome and beyond: diverse evolutionary consequences of mating system transitions in plants

“…Mazer et al [96] found that the selfing taxon had smaller seeds than outcrossers in each taxon pair, while the local climate was also associated with seed size [96]. Second, a largescale statistical analysis using 642 species from three plant families revealed that selfing species generally have smaller seed mass compared with outcrossing congeners, by controlling for possible confounding factors such as phylogeny and growth forms [97]. These results are consistent with the parental conflict hypothesis, but there are also non-mutually exclusive alternative hypotheses, such as colonization ability, which should be associated with both selfing and small seeds, and the prediction of sex allocation theory, in which the P/O ratio should increase linearly with increasing seed mass among seeding plants [98].…”

The evolutionary dynamics of plant mating systems: how bias for studying ′interesting′ plant reproductive systems could backfire

“…Papers which address the interplay of selfing at a multi-family level with other various topics in ecology and evolution have been especially prolific. For example, selfing has been explored in conjunction with geographic range dynamics (Grossenbacher et al 2015(Grossenbacher et al , 2016, invasive status and naturalization (Rananjatovo et al 2016), island biogeography (Grossenbacher 2017), within-population selfing rate variation (Whitehead et al 2018), life history and range size (Prior and Busch 2021), and seed size (Tateyama et al 2021). Additionally, studies focused on estimating rates of transitions to and from selfing using phylogenetic comparative methods (PCMs) have contributed significantly to knowledge about the tempo and mode of selfing evolution.…”

Population size as a major determinant of mating system and population genetic differentiation in a narrow endemic chasmophyte

“…The change from allogamy (geitonogamy and xenogamy) to autogamous self-fertilisation is usually associated with a selfing syndrome – a characteristic set of changes in floral morphology and function that promote autonomous selfing [ 16 , 29 ]. As has been demonstrated in a number of plant genera, predominantly selfing species have less conspicuous floral display in the form of a smaller number and size of flowers and fewer simultaneously open flowers than their outbreeding relatives [ 5 , 30 , 31 ], smaller and lighter seeds [ 32 – 35 ], reduced pollen-to-ovule ratio [ 36 ], and lower nectar and scent production [ 37 – 40 ].…”