Pollination ecotypes and the origin of plant species

Abstract

Ecological niche shifts are a key driver of phenotypic divergence and contribute to isolating barriers among lineages. For many groups of organisms, the history of these shifts and associated trait-environment correlations are well-documented at the macroevolutionary level. However, the processes that generate these patterns are initiated below the species level, often by the formation of ecotypes in contrasting environments. Here, I review the evidence in plants for 'pollination ecotypes' as microevolutionary responses to environmental gradients in pollinator availability. Pollinators are critical for population establishment and persistence in most species, thereby forming part of their fundamental niche. Novel floral trait combinations allow species to exploit particular pollination opportunities in local habitats and evolve primarily through sexual selection due to their effects on mating success. I examine selected case studies on the evolution of pollination ecotypes, including self-pollinating forms, and use these to illustrate challenging practical and conceptual issues. These issues include the paucity of reliable natural history data, the problem of implementing and interpreting reciprocal translocation experiments, and establishing criteria for when allopatric ecotypes should be considered species.

Keywords: floral syndromes; local adaptation; mutualism; pollination; range limits; speciation.

Figure 1.

Examples of pollination ecotypes. (a,b) Platanthera bifolia (Orchidaceae); long-spurred ecotype (a) pollinated by the hawkmoth Sphinx ligustri and shorter-spurred ecotype (b) pollinated by the hawkmoth Hyloicus pinastri [76]. (c,d) Gladiolus longicollis (Iridaceae); short-tubed form (c) pollinated by short-proboscid hawkmoths and long-tubed ecotype (d) pollinated by long-proboscid hawkmoths [62]. (e,f) Eulophia parviflora (Orchidaceae); spurless ecotype pollinated by beetles (e) and spurred ecotype (f) pollinated by solitary bees [77]. (g,h) Disa ferruginea (Orchidaceae); butterfly-pollinated orange-flowered ecotype (left) and red-flowered ecotype (right) [78]. (h,i) Mimulus aurantiacus. (Phrymaceae); yellow-flowered ecotype pollinated by hawkmoths (h) and red-flowered ecotype pollinated by hummingbirds [63]. (j) Erica plukenetii (Ericaceae); long-tubed ecotype pollinated by malachite sunbirds (left), medium-tubed ecotype pollinated by orange-breasted sunbirds (centre) and short-spurred ecotype pollinated by noctuid moths (right) [60]. (k). Primula oreodoxa complex (Primulaceae); P. oreodoxa short-styled morph (left), P. oreodoxa homostylous morph (centre) and homostylous P. dumicola (right) [37]. (l,m) Eichhornia paniculata (Pontederiaceae); short-styled morph (l) and semi-homostylous morph (m) [79]. Scale bars (a–j) = 10 mm, (k–m) = 5 mm. Photo credits: Steve Johnson (a–g), Matt Streisfeld (h,i), Timo van der Niet (j), Wei Zhou (k) and Spencer Barrett (l,m).

Figure 2.

A schematic representation of the process of speciation through progressive intermediate stages of ecotype formation. Initial allopatry or parapatry of population clusters allows local adaptation to various environmental conditions. Resulting ecotypes can merge back into parental lineages, become extinct or persist to diverge further, ultimately becoming species. The sequences of adaptations shown are hypothetical and in some cases are confined to one lineage, as expected in peripatric divergence. Note that species 1 and 2 could also be interpreted as ecotypes of a single species. Adapted from van der Niet et al. [25].