Organisms on islands experience unique selective regimes that may lead to unconventional changes in ecologically important traits. For example, the majority of flowers in oceanic islands have unspecialized floral phenotypes (Carlquist, 1974; Webb & Kelly, 1993), suggesting that shifts to generalization have been common in the evolutionary history of island plants. By contrast, transitions from generalized to specialized or between specialized pollination systems are the most frequently reported patterns in studies of floral evolution conducted primarily on mainland plant taxonomic groups (reviewed in Weller & Sakai, 1999; Fenster et al., 2004; Tripp & Manos, 2008). This study provides the first evidence supported by pollination ecology data, for evolutionary transitions towards generalized pollination in a plant group from the Caribbean islands. At the same time, there is evidence for diversification of specialized hummingbird and bat-pollinated lineages. Below we examine patterns of pollination and breeding system evolution for the tribe Gesnerieae, and discuss how simultaneous study of both aspects of plant reproduction within the context of phylogeny can provide important insights for floral evolution.
Suites of correlated floral traits or ‘pollination syndromes’, are generally believed to reflect convergent selection pressures exerted by one functional group of pollinators (Faegri & van der Pjil, 1978). The results of this study support our previous findings in support of classic bat and hummingbird pollination syndromes in a nonphylogenetically corrected study of the Gesnerieae (Martén-Rodríguez et al., 2009). Additionally this study revealed that in Antillean Gesnerieae, pollination system transitions occur either by switching pollinator functional groups (for example, hummingbird to bat), or by adding different functional groups (e.g. bats and insects).
The evolution of bat pollination in Gesnerieae involves changes in flower color, timing of anther dehiscence (Fig. 4), and timing and quantity of nectar production. The latter trait was not mapped onto the phylogeny because of the small number of species for which daily nectar production was quantified. However, where these estimates are available, nectar volume averages 12.5 μl (± 3.99, n = 3) for hummingbird-pollinated species, 75.2 μl (± 14.85, n = 2) for bat-pollinated species, and 67.1 μl (± 7.55, n = 3) for generalists (Martén-Rodríguez & Fenster, 2008; A Almarales-Castro & S Martén-Rodríguez, unpublished). High nectar production and floral scent are considered important attractants in bat-pollinated flowers, including members of the Gesneriaceae family (Sazima et al., 1999; Tschpka & Dressler, 2002); however, tribe Gesnerieae species have no distinguishable floral scent. Lack of scent in bat-pollinated Gesnerieae may be indicative of recent origins of chiropterophilous flowers from odorless hummingbird-pollinated ancestors and illustrates how fit to classic pollination syndromes is often incomplete due to genetic or historical constraints.
The evolution of generalized pollination by bats, moths and hummingbirds in Gesnerieae was associated with the evolution of subcampanulate corollas. Other floral traits in these species probably reflect adaptation to both hummingbirds and nocturnal pollinators. For instance, broad corolla openings, schedules of anther dehiscence and nectar production reflect selection by nocturnal pollinators. However, the constriction above the nectar chamber and red markings on yellow corollas appear to reflect selection by hummingbirds. In particular, the corolla constriction may promote contact of the hummingbird’s bill with the reproductive organs of the flower (Martén-Rodríguez et al., 2009), an idea that needs to be empirically tested. In generalized Gesnerieae, hummingbird visits occur both in late afternoon, when nectar production starts, and during early morning hours (Martén-Rodríguez et al., 2009). However, since pollen is mostly unavailable until c. 18:00 h, hummingbirds should be most effective at dawn, particularly when nocturnal pollination has failed. Under this scenario, generalization may provide a mechanism for reproductive assurance where pollinator service by bats is low.
Studies of other plant species that share bat and hummingbird pollination are inconclusive as to whether intermediate traits represent transitional phenotypes, or phenotypes adapted to both functional pollinator groups (e.g. Abutilon, Buzato et al., 1994; Syphocampylus sulfureus, Sazima et al., 1994). It has been suggested that a stage of greater generalization is likely to occur between transitions among specialized pollination systems (Baker, 1963; Wilson et al., 2006). The fact that even specialized flowers are often visited by a number of the potential pollinators present in a community would allow selection by different floral visitors to operate at a given time and space (Baker, 1963). During a transitional stage, floral phenotypes would reflect these different selective pressures, as suggested for some species of Penstemon (bird- and bee-pollinated, Wilson et al., 2006). However, under certain ecological conditions a particular pollinator group may become more important and drive floral specialization in an alternate direction (Baker, 1963).
In Gesnerieae, floral change driven by the pollinator environment is exemplified in the lineage of generalists, including Rhytidophyllum grandiflorum and R. vernicosum. Both species occur at high elevations (> 1500 m) in the Dominican Republic, where nectar-feeding bats are absent or rare. While R. grandiflorum maintains nocturnal schedules of anther dehiscence and nectar production, R. vernicosum shows a mixed phenotype with diurnal and nocturnal schedules (i.e. plants and flowers within plants vary in the amount of red pigmentation in corollas, and in the schedules of nectar production and anther dehiscence). R. vernicosum has a higher frequency of hummingbird visitation than other generalists, and successful pollen deposition is facilitated by strong corolla curvature. Moths also contribute to pollination in this species (Martén-Rodríguez et al., 2009; S Martén-Rodríguez, unpublished). Overall, these findings suggest that R. vernicosum may represent a transitional generalized stage reverting to hummingbird pollination.
Based on the current phylogenetic hypothesis and stochastic mapping of characters, reversals to hummingbird pollination are rare in Gesnerieae. This result parallels findings of other studies where pollinator transitions are labile only in certain directions, for example, bee to hummingbird in Costus (Kay et al., 2005) and Penstemon (Wilson et al., 2007), ornithophilous to chiropterophilous flowers in Sinningieae (Perret et al., 2003), and diurnal to nocturnal pollination in Ruellia (Tripp & Manos, 2008). Possible causes for these unidirectional trends are: environmental constraints (e.g. the effectiveness of available pollinators; Wilson et al., 2007), or internal constraints (e.g. physiological limitations; Rausher, 2008). For example, the evolution of nocturnal pollination frequently involves loss of red pigmentation. This floral transition has been associated with ‘loss of function’ mutations in the pathway of anthocyanin production (Mol et al., 1998), which makes loss of red color difficult to regain (Whittall et al., 2006; Rausher, 2008). However, physiological constraints do not satisfactorily explain the case of Gesnerieae, since the ability to produce red floral pigments is not lost in all lineages of generalist and bat-pollinated species (Figs 1, 6). The directionality of transitions in Gesnerieae is likely determined by a combination of historical factors (i.e. hummingbird-pollinated flowers are ancestral), environmental constraints (e.g. low hummingbird visitation), and internal constraints (e.g. the ability to evolve self-pollination mechanisms for reproductive assurance and inbreeding history).
Breeding system evolution
Autonomous self-pollination is thought to provide reproductive assurance in many angiosperm species across a wide range of floral morphologies and pollination systems (Lloyd, 1992; Fenster & Martén-Rodríguez, 2007). In Gesnerieae, autonomous self-pollination occurs in three independent lineages, all of which are hummingbird-pollinated (Fig. 7). Ecological studies suggest that this association was promoted by the low and unpredictable pollinator service by hummingbirds in the Caribbean islands. Three findings support this assertion: first, hummingbird-pollinated species have the lowest frequencies of pollinator visitation (mean number of visits per flower d−1 = 1 ± 1.5 SE, n = 9) when compared with bat-pollinated (2 ± 1.8, n = 5) and generalist species (13 ± 1.8, n = 5), where n = number of observed species (Martén-Rodríguez et al., 2009); second, significant pollen limitation (higher fruit set of hand-pollinated vs open-pollinated plants) was detected only in specialized species (Martén-Rodríguez & Fenster, 2010); third, autonomous self-pollination provides reproductive assurance in three out of four studied hummingbird-pollinated Gesnerieae (Martén-Rodríguez & Fenster, 2010). Overall, these findings suggest that inadequate pollinator service underlies the evolution of autonomous self-pollination in ornithophilous Gesnerieae as a strategy to mitigate pollen limitation and ensure seed production when vector-mediated pollination fails. This rationale, however, does not explain why bat-pollinated Gesnerieae, which are also pollen-limited, have not evolved reproductive assurance mechanisms.
Could the observed pattern of breeding system evolution be the result of differential expression of dichogamy among hummingbird- and bat-pollinated species? Protogyny provides a more intuitive mechanism for reproductive assurance because self-pollination can occur at the end of the receptivity period (Bertin & Newman, 1993; Mallick, 2001). However, although protogyny tends to be associated with self-compatibility (Routley et al., 2004), a general association of protogyny with autonomous selfing mechanisms has not been demonstrated (Fenster & Martén-Rodríguez, 2007). In Gesnerieae, autonomous selfing has evolved only in protogynous lineages, but the evolution of animal pollination systems is not associated with shifts in dichogamy (e.g. origins of protandry occur both in hummingbird- and bat-pollinated lineages, Fig. 7). Thus, the results indicate that expression of dichogamy is not responsible for variation in reproductive assurance mechanisms among Gesnerieae species.
An alternative explanation is that autonomous pollen transfer is related to flower shape. In tubular corollas the reproductive organs are in close proximity, making autonomous deposition of self-pollen on stigmas more likely. This idea is supported by a study of South American Schizanthus (Solanaceae), where autonomous self-pollination has evolved only in tubular-flowered species pollinated by hummingbirds or moths (Perez et al., 2006). Thus, the positioning of the reproductive organs in narrow corollas may constitute a preadaptation to the evolution of the reproductive assurance mechanisms by increasing the precision of self-pollen deposition (Mazer & DeLesalle, 1998).
A unified view of pollination and breeding system evolution: what is special about islands?
Pollination systems in islands show a great proportion of generalized interactions (Olesen et al., 2002), and high frequency of wind pollination (Bernardello et al., 2001). Pollinator-depauperate faunas on islands are thought to be responsible for these trends. First, reduced interspecific competition may cause island species to have broader feeding niches than their mainland relatives (Olesen et al., 2002). For example, in the Dominican Republic, hummingbirds are represented by only three species, one of which is so small that it cannot access nectar from typical ornithophilous flowers. Thus, a single hummingbird species may be responsible for the pollination of all ornithophilous plant species in certain communities. Additionally, and perhaps related to low species diversity, visitation frequencies on islands are often lower than in mainland regions (Linhart & Feinsinger, 1980; Martén-Rodriguez et al., 2009).
Under conditions of low pollinator service, natural selection should favor reproductive strategies that reduce the risk of pollination failure on islands. For instance, the ability to self may partly explain the maintenance and diversification of hummingbird lineages in the Antilles. The results of this study support the idea that low diversity of pollinator species on islands select for generalization and autogamy as reproductive assurance mechanisms. Our findings highlight the importance of simultaneously studying pollination and breeding system evolution to achieve a comprehensive understanding of the processes underlying floral diversification.