Behavioural environments and niche construction: the evolution of dim‐light foraging in bees

Abstract

Most bees forage for floral resources during the day, but temporal patterns of foraging activity vary extensively, and foraging in dim-light environments has evolved repeatedly. Facultative dim-light foraging behaviour is known in five of nine families of bees, while obligate behaviour is known in four families and evolved independently at least 19 times. The light intensity under which bees forage varies by a factor of 10 8 , and therefore the evolution of dim-light foraging represents the invasion of a new, extreme niche. The repeated evolution of dim-light foraging behaviour in bees allows tests of the hypothesis that behaviour acts as an evolutionary pacemaker. With the exception of one species of Apis, facultative dim-light foragers show no external structural traits that are thought to enable visually mediated flight behaviour in low-light environments. By contrast, most obligate dim-light foragers show a suite of convergent optical traits such as enlarged ocelli and compound eyes. In one intensively studied species (Megalopta genalis) these optical changes are associated with neurobiological changes to enhance photon capture. The available ecological evidence suggests that an escape from competition for pollen and nectar resources and avoidance of natural enemies are driving factors in the evolution of obligate dim-light foraging.

Photic niche invasions: phylogenetic history of the dim-light foraging augochlorine bees (Halictidae)

“…As with diurnal bees, manipulation of horizontal flow in the visual field alters flight speed in Megalopta, even at low light intensities [47]. In addition, Megalopta possess a number of other neuro-physiological and anatomical adaptations for vision in dim light (reviewed by Wcislo & Tierney [17] and Warrant [21]). Future research aims to link these adaptations with studies of opsin expression.…”

“…Megalopta bees use more than 60 angiosperm species at one site in central Panama (I. Lopez, A. R. Smith & W. Wcislo 2007, unpublished data), but little is known of their role as potential pollinators. Hopkins et al [64] noted that Megalopta was the most abundant visitor to Parkia velutina in Brazil, and hypothesized that nocturnal bees may have played a role in opening a new niche (night-blooming flowers), which was subsequently exploited by bats (for a more detailed discussion, see [17]). …”

“…dS) within all gene fragments that were used to construct the phylogeny. Then we compared LwOp by foraging mode across our dataset, as well as independent pairwise analyses among 11 pairs of bee taxa with nocturnal versus diurnal foraging behaviour, for which comparable sequences are available (listed in the electronic supplementary material, table S1); behavioural categorizations were taken from Wcislo & Tierney [17].…”

“…Here we explore the phylogenetic history of the obligate dim-light foraging augochlorine sweat bees (Megalopta, Megaloptidia and Megommation), the most diverse radiation of dim-light bees within the Apoidea (reviewed by Wcislo & Tierney [17]). These bees forage under light conditions that are orders of magnitude dimmer than related diurnal taxa [18 -20] (reviewed by Wcislo & Tierney [17] and Warrant [21]), so there are reasons to expect that augochlorine opsin proteins may be under strong selection that led to adaptive radiations, as in other taxa such as cichlid fishes [8,22].…”

“…These bees forage under light conditions that are orders of magnitude dimmer than related diurnal taxa [18 -20] (reviewed by Wcislo & Tierney [17] and Warrant [21]), so there are reasons to expect that augochlorine opsin proteins may be under strong selection that led to adaptive radiations, as in other taxa such as cichlid fishes [8,22]. If so, opsin may be unsuitable for our phylogenetic purposes, which we test by comparison with two non-photic nuclear protein-coding genes.…”