(Coleoptera: Lampyridae) and Evolution of the Opsin Genes Underlying Color Vision
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Org Divers Evol (2015) 15:513–526 DOI 10.1007/s13127-015-0212-z ORIGINAL ARTICLE Review of the firefly visual system (Coleoptera: Lampyridae) and evolution of the opsin genes underlying color vision Gavin J. Martin1 & Nathan P. Lord1 & Marc A. Branham2 & Seth M. Bybee1 Received: 23 October 2014 /Accepted: 10 April 2015 /Published online: 28 April 2015 # Gesellschaft für Biologische Systematik 2015 Abstract Among insects, opsin copy number variation has Keywords Phylogeny . Coleoptera . Lampyridae . Opsin . been shown to be quite diverse. However, within the beetles, Transcriptome . Bioluminescence very little work on opsins has been conducted. Here, we look at the visual system of fireflies (Coleoptera: Lampyridae), which offer an elegant system in which to study visual evolu- Introduction tion as it relates to their behavior and broader ecology. They are the best-known case of a terrestrial organism that commu- Vision plays a central role in the lives of most animals. From nicates through the use bioluminescence. The molecular basis predator avoidance to prey detection, from mate to habitat for this communication is relatively simple: one gene family selection, the ability to sense one’s surroundings using visual (opsins) controls the detection of the signal, and one gene cues has long fascinated scientists (Warrant and Nilsson family (luciferase) controls the production of the signal. We 2006). The components of visual communication between use a transcriptomic approach to sample for and investigate animals can be extremely complicated for scientists to tease opsin evolution in fireflies. We also use a phylogenetic esti- apart. When one considers the need for animals to discrimi- mate of Lampyridae to examine the evolution and ancestral nate what signal is being transmitted, what medium or media modality of adult courtship communication. We find evidence the signal is being transmitted through, and how the signal is for only two expressed opsin classes in each of the nine firefly being perceived, there are so many variables that the study of species studied, one in the ultraviolet-sensitive and one in the vision in its totality can seem daunting. However, the presence long-wavelength-sensitive areas of the visible spectrum. Bio- of visual pigments allows for a more direct, preliminary ex- luminescent communication in adults is not optimized to be amination and understanding of visual communication. Visual present ancestrally, and was gained two times with six subse- pigments are composed of an opsin protein covalently bound quent losses. Despite the need for most adult fireflies to re- to a chromophore, the specific molecule responsible for light spond to a clearly sexual and colorful visual signal absorption (Wald 1967), and are contained within the photo- (bioluminescence) to maximize fitness, their visual system is receptor cells of the eye. Opsins are responsible for light de- relatively simple, and does not match the trend for opsin du- tection and overall vision, but multiple opsin copies can allow plication found in other insect groups. for color discrimination. Color discrimination is achieved by comparing the given stimulation of one opsin with another opsin that is sensitive to a different portion of the visible light spectrum (Cuthill 2006). There are currently four known * Gavin J. Martin Btypes or groups^ of opsin: C-type, R-type, Cnidops, and [email protected] Group 4 (Porter et al. 2012). Here, we restrict our discussion to only the R-type opsins, which are largely responsible for 1 Department of Biology, 4102 LSB, Brigham Young University, arthropod vision. Changes in the amino acid sequence of the Provo, UT 84602, USA opsin protein or in the structure of the chromophore can alter 2 Department of Entomology & Nematology, University of Florida, the overall spectral sensitivity of these pigments. The number P.O. Box 110620, Gainesville, FL 32611, USA of expressed opsins and the range in sensitivity is known to 514 G.J. Martin et al. vary across animals (Rivera and Oakley 2009; Briscoe and underlying molecular systems may also exhibit equal degrees Chittka 2001; Land and Nilsson 2012). For example, in sto- of variability (Rivera and Oakley 2009). This is best tested in matopods (Crustacea), 6–15 different expressed opsins have those lineages in which it is clear that visual communication been found (Porter et al. 2009). plays an important role in life history. Perhaps one of the best Arthropods, specifically insects, are the most diverse group examples of a visual coleopteran is the firefly (lightning bug; of animals on earth, and their visual systems reflect this diver- family Lampyridae), easily recognizable for their biolumines- sity (Rivera and Oakley 2009). Three major opsin classes have cent flash patterns, which are used to communicate both inter- been identified in insects: ultraviolet-sensitive (UVS), blue- and intra-specifically. sensitive (BS) and long-wavelength-sensitive (LWS). Based Fireflies are arguably the most well-known bioluminescent on a phylogenetic analysis of 54 arthropod species, it is hy- organism in the animal kingdom. In the marine environment, pothesized that the ancestral state for insect vision is a single particularly in the deep ocean, examples of bioluminescence copy of each of the three classes (Briscoe and Chittka 2001). are prolific and found among many lineages of organisms, but However, current research demonstrates varying numbers of terrestrial examples are comparatively rare in scope and diver- copies within each of these classes. In Panorpa cognata sity. Light production in fireflies is hypothesized to have orig- Rambur (Mecoptera), there is evidence for only one opsin inated as an aposematic warning signal among larvae (LWS; Burkhart and De LaMotte 1972, K. Manwaring unpub- (Branham and Wenzel 2001, 2003). Many fireflies are chem- lished data), while in Papilio glaucus Linnaeus (Lepidoptera) ically defended by distasteful steroids called lucibufagins six total opsin copies across the three classes have been recov- (Eisner et al. 1978) that are likely advertised via biolumines- ered (Briscoe 2000). Some dragonflies appear to have at least cence (Crowson 1972;Sivinsky1981; Underwood et al. 1997; five copies across the three classes (Yang and Osorio 1991), De Cock and Matthysen 2003; Branham 2010). It is hypoth- with some species having as many as three LWS opsin copies esized that this aposematic, larval bioluminescence was then alone (Bybee unpublished data; Meinertzhagen et al. 1983. co-opted as a method of adult visual communication Other insects (e.g., beetles, Tribolium castaneum (Herbst); (Branham and Wenzel 2003). In addition to bioluminescence, owlflies, Ascalaphus macaronius Scopoli; cockroaches, many fireflies also use pheromones to communicate as adults Periplaneta americana Linnaeus) appear to have lost the blue and several different sexual communication systems have opsin class entirely (Briscoe and Chittka 2001; Jackowska been proposed that incorporate different degrees of biolumi- et al. 2007;Gogala1967;Pauletal.1986; Mote and Gold- nescence and/or pheromones (see Table 1 for review). smith 1970). Bioluminescent emission data, as well as peak spectral sen- Given the large diversity in opsin copy number across in- sitivity, has been recorded for several firefly species (Fig. 1) sects, and especially within the hyper-diverse Holometabola (Lall 1981;Lalletal.1980, 1988;Eguchietal.1984;Lalland (Diptera, Lepidoptera, and Hymenoptera), we expect a similar Worthy 2000). In all but one firefly species, Photinus pyralis diversity in beetles (Coleoptera). Surprisingly, opsins do not (Linnaeus), the peak wavelength in visual sensitivity is within appear to have diversified across beetles as in other holome- 5 nm of the peak intensity of the emission. Eguchi et al. (1984) tabolous insect groups, but to date opsin copy variation for suggested that while the luciferase emission peak is in concor- relatively few beetles has been studied. Only one copy of the dance with peak spectral sensitivity, especially in his study of LWS and one copy of the UVS were recovered in the red flour Japanese fireflies, this does not mean that the opsin is specif- beetle T. castaneum (Jackowska et al. 2007). However, ically tuned to the emission; rather, it suggests that the emis- Maksimovic et al. (2009) recovered three copies (two UVS sion of particular wavelengths evolved to take advantage of a and one LWS) in the larval stage of the sunburst diving beetle pre-existing spectral sensitivity. Thus, an important question is Thermonectus marmoratus (Gray) and Crook et al. (2009) how diversity between opsin(s) and luciferase(s) are found electroretinographic (ERG) evidence for four sensitivi- interlinked. ties in the emerald ash borer Agrilus planipennis Fairmaire. It Oba and Kainuma (2009) found a correlation between op- is important to note that ERG data does not necessarily corre- sin expression and time of day in Luciola cruciata late one-to-one with opsin number (see below). The beetles Motschulsky. L. cruciata was found to have two expressed are a cosmopolitan group of extraordinarily diverse insects opsin classes—one in the UVS (360 nm) and one in the that occupy a vast number of ecological niches, both terrestrial LWS (560 nm) portions of the spectrum. In male L. cruciata, and aquatic. Coleoptera exhibit a range of eye types from neither UVS nor LWS opsin expression varied significantly anophthalmy (loss), to microphthalmy (reduction), to simple throughout the day. In