How exaptations facilitated photosensory evolution: Seeing the light by accident

Abstract

Exaptations are adaptations that have undergone a major change in function. By recruiting genes from sources originally unrelated to vision, exaptation has allowed for sudden and critical photosensory innovations, such as lenses, photopigments, and photoreceptors. Here we review new or neglected findings, with an emphasis on unicellular eukaryotes (protists), to illustrate how exaptation has shaped photoreception across the tree of life. Protist phylogeny attests to multiple origins of photoreception, as well as the extreme creativity of evolution. By appropriating genes and even entire organelles from foreign organisms via lateral gene transfer and endosymbiosis, protists have cobbled photoreceptors and eyespots from a diverse set of ingredients. While refinement through natural selection is paramount, exaptation helps illustrate how novelties arise in the first place, and is now shedding light on the origins of photoreception itself.

A putative origin of the insect chemosensory receptor superfamily in the last common eukaryotic ancestor

“…These genes might have been independently lost in many lineages and/or have diverged beyond sequence-based homology detection levels. It is also possible that some homologs were acquired by lateral gene transfer, as has been proposed to explain the patchy phylogenetic distribution of microbial rhodopsins ( Gavelis et al, 2017 ).…”

Light-Induced Stress as a Primary Evolutionary Driver of Eye Origins

“…In fact, explicit calculations of the physical and optical requirements for the different sensory tasks match well with physical capabilities inferred from the increasingly complex morphologies (Nilsson 2013). These functional categories also hold outside animals, in various single-celled organisms (Colley and Nilsson 2016;Gavelis et al 2017;Swafford and Oakley 2018) While the gradual elaboration of eyes may be explained by selection on visual function, it is unclear how each of these parts originated before selective pressures to refine visual acuity could shape their evolutionary trajectories (Oakley and Pankey 2008). Besides gradual modifications like deepening of pigment cups and elaboration of lenses, the complexification of eyes required discrete steps, including origins of photoreception, origins of pigmentation adjacent to photoreceptors, and origins of lens-like material in the path of light.…”

A putative origin of insect chemosensory receptors in the last common eukaryotic ancestor

“…The extremely sparse phylogenetic distribution of these genes in unicellular eukaryotes suggests that they have been independently lost in many lineages, although we may have missed distant homologues despite our efforts to perform exhaustive searches. It is also possible that some homologues were acquired by lateral gene transfer, as has been proposed to explain the patchy phylogenetic distribution of microbial rhodopsins (Gavelis, et al 2017). The global conservation of the structural features of unicellular eukaryotic GRLs and DUF3537 proteins with insect chemosensory receptors argues that they might also be ligand-gated ion channels.…”