Long‐tongued insects promote disassortative pollen transfer in style‐dimorphic Narcissus papyraceus (Amaryllidaceae)

Abstract

Summary1. In hermaphroditic flowers, reciprocal herkogamy, for example heterostyly, enhances pollen transfer between floral morphs (disassortative pollination) while avoiding self-interference between sexual organs. By contrast, disassortative pollination might be compromised in style-dimorphic flowers, which lack perfect reciprocity between the two floral morphs. This suboptimal functioning has been considered to explain why stylar dimorphism is rare in nature.2. Some style-polymorphic species receive a wide array of floral visitors, including long-tongued insects that feed on nectar and short-tongued insects that feed on pollen. Differences in the morphology and behaviour of these two insect types could be manifested as different pollination patterns in each floral morph.3. By observing individual pollinators and pollen deposition and delivery in small field-based experimental arrays with emasculated and intact flowers, we studied pollination patterns mediated by different insect types (long-and short-tongued) in the two floral morphs (long-and short-styled) of the style-dimorphic Narcissus papyraceus. We investigated the patterns of pollen transfer between and within style morphs in cross-pollinations, as well as self-pollination and pollen removal rates, for each floral morph mediated by each insect type.4. Long-tongued insects were efficient pollinators of both floral morphs as they removed little pollen from the anthers but deposited comparatively large amounts on the stigmas. Although disassortative pollen transfer and assortative pollen transfer were equally high to the long-styled morph, the former prevailed in the short-styled morph. Short-tongued insects removed large amounts of pollen from the anthers but deposited only a few pollen grains on the long-styled stigmas and a negligible number of grains on short-styled stigmas regardless of the morph of the donor. 5.Synthesis. In this study, we provide empirical support for the hypothesis that, under the action of long-tongued pollinators, pollen transfer patterns in the stylar-dimorphic Narcissus papyraceus resemble in part those of heterostylous species. In addition, we found that short-tongued insects act mostly as pollen thieves, thereby limiting the male fitness of both style morphs, besides depleting the female fitness of S-morph plants. In view of these results, we propose that the differing pollination efficiencies of floral visitors, in addition to their frequency, are key in determining the morph ratio of populations in this Narcissus.

Associations between sex‐organ deployment and morph bias in related heterostylous taxa with different stylar polymorphisms

“…3G ). Elsewhere among heteromorphic plants, high levels of disassortative mating resulting in equal morph ratios have been reported in self-compatible, tristylous Eichhornia paniculata ( Barrett et al, 1987 ;Kohn and Barrett, 1992 ) and in stylar dimorphic Narcissus papyraceus ( Simón-Porcar et al, 2014, 2015a. We observed abundant pollinator visitation by long-tongued bees in distylous Glandora and Lithodora populations ( Ferrero et al, 2011b ) and these insects probably play a key role in promoting disassortative mating and causing isoplethic morph ratios.…”

“…For example, in stigma dimorphic Narcissus assoanus , both L-morph biased and isoplethic populations are reported in southern France and these differ in size and the quantity and quality of pollinator service ( Baker et al, 2000a , c ). Diff erences in the types of pollinators visiting populations of other stigma-height dimorphic Narcissus species have also been implicated in causing variation in morph ratios ( Arroyo and Dafni, 1995 ;Simón-Porcar et al, 2014 ). A theoretical model of pollination and mating in stigma-height dimorphic populations, based on empirical data on the fl oral biology of Narcissus species, demonstrated that greater assortative mating in the L-morph, because of the reduced herkogamy of this morph compared to the S-morph, could explain the L-biased populations that are most commonly encountered in this genus ( Baker et al, 2000a ).…”

“…However, stigma-height dimorphism is clearly a stable polymorphism in each of these taxa because it is reported from a signifi cant number of species. Moreover, at least in Narcissus , there is experimental evidence that despite incomplete sexorgan reciprocity and intramorph compatibility, disassortative mating is promoted by stigma-height dimorphism ( Simón-Porcar et al, 2014, 2015a, and the stylar morphs are subject to frequencydependent selection ( Th ompson et al, 2003 ) in the same manner as in distylous populations.…”

Phenotypic integration in style dimorphic daffodils (Narcissus, Amaryllidaceae) with different pollinators

“…Shifts from long-to short-tongued pollinators seem to select against the S morph and favour the L morph [59,60]. Thus, a steeper fitness surface could be expected in populations where flowers have close fit with pollinators (long-tongued insects) than in populations in which pollinators fit loosely with flowers (short-tongued insects), and this should be reflected in the patterns of phenotypic integration [2,18].…”

“…Furthermore, differences between population types in the average correlation between anther height and flower tube length were larger for the lower anther level than the upper anther level. This may reflect two processes that are not mutually exclusive: (i) selection generated by LT-pollinators for a precise position of the lower anther level to donate pollen to S-stigmas in dimorphic populations [58,92]; and/or (ii) relaxation of selection on the lower anther level in L-monomorphic populations because, unlike long-tongued insects, short-tongued pollinators interact only with the upper anther level (R Pérez-Barrales 2003, personal observation; [60]). …”