The evolution of plant reproductive systems: how often are transitions irreversible?

Abstract

Flowering plants are characterized by striking variation in reproductive systems, and the evolutionary lability of their sexual traits is often considered a major driver of lineage diversification. But, evolutionary transitions in reproductive form and function are never entirely unconstrained and many changes exhibit strong directionality. Here, I consider why this occurs by examining transitions in pollination, mating and sexual systems, some of which have been considered irreversible. Among pollination systems, shifts from bee to hummingbird pollination are rarely reversible, whereas transitions from animal to wind pollination are occasionally reversed. Specialized pollination systems can become destabilized through a loss of pollinator service resulting in a return to generalized pollination, or more commonly a reliance on selfpollination. Homomorphic and heteromorphic self-incompatibility systems have multiple origins but breakdown to self-compatibility occurs much more frequently with little evidence for subsequent gains, at least over short time-spans. Similarly, numerous examples of the shift from outcrossing to predominant self-fertilization are known, but cases of reversal are very limited supporting the view that autogamy usually represents an evolutionary dead-end. The evolution of dioecy from hermaphroditism has also been considered irreversible, although recent evidence indicates that the occurrence of sex inconstancy and hybridization can lead to the origin of derived sexual systems from dioecy. The directionality of many transitions clearly refutes the notion of unconstrained reproductive flexibility, but novel adaptive solutions generally do not retrace earlier patterns of trait evolution.

Different patterns of colonization of Oxalis alpina in the Sky Islands of the Sonoran desert via pollen and seed flow

“…Recent studies have investigated the influence of historical processes such as vicariance events related to climatic changes on the evolutionary dynamics of the plant breeding systems (Dorken & Barrett, 2004; Hodgins & Barrett, 2007; Pérez‐Alquicira et al., 2010; Zhou, Barrett, Wang, & Li, 2012). Furthermore, selective pressures associated with the immobility of plants and their reliance on pollen vectors have played an important role in the expression of breeding system variability (Barrett, 2013). …”

Dioecious plants are more precocious than cosexual plants: A comparative study of relative sizes at the onset of sexual reproduction in woody species

“…Despite the potential disadvantages, 43% of angiosperm families have dioecious members (Renner, 2014; Renner & Ricklefs, 1995), and the evolution of dioecy has occurred independently many times across a diverse range of taxonomic groups (Barrett, 2013; Renner, 2014). Furthermore, dioecious plant species occur in global plant communities, although tropical or island flora has higher incidences of dioecious species compared to the global proportion of 6% (Bawa, 1980; Ibarra‐Manriquez & Oyama, 1992; Queenborough et al., 2009; Sakai, Wagner, Ferguson, & Herbst, 1995a; Vary et al., 2011).…”

Causes and evolutionary consequences of primordial germ-cell specification mode in metazoans

“…Germ plasm thus appears to follow "Dollo's Law"-that is, structures or processes lost in evolution are unlikely to be regained by descendants in the same form as the ancestors (67,68). In this aspect, the inheritance mode resembles other typically irreversible transitions, such as the transition from outcrossing to selfing and from hermaphroditism to dioecy (69). In plants, for example, the shift from blue to red flowers in Andean Iochroma (Solanaceae) is irreversible; molecular studies suggest that loss of a gene encoding an enzyme in the anthocyanin pathway is needed for the transition, which limits the opportunity for later reversal to the ancestral state (69,70).…”

“…In this aspect, the inheritance mode resembles other typically irreversible transitions, such as the transition from outcrossing to selfing and from hermaphroditism to dioecy (69). In plants, for example, the shift from blue to red flowers in Andean Iochroma (Solanaceae) is irreversible; molecular studies suggest that loss of a gene encoding an enzyme in the anthocyanin pathway is needed for the transition, which limits the opportunity for later reversal to the ancestral state (69,70). Accordingly, the transition from induction to inheritance could, in principle, be made irreversible by a single gene mutation or gene loss in the induction pathway.…”