Variation in opsin genes correlates with signalling ecology in North American fireflies

Abstract

Genes underlying signal reception should evolve to maximize signal detection in a particular environment. In animals, opsins, the protein component of visual pigments, are predicted to evolve according to this expectation. Fireflies are known for their bioluminescent mating signals. The eyes of nocturnal species are expected to maximize detection of conspecific signal colors emitted in the typical low-light environment. This is not expected for species that have transitioned to diurnal activity in bright daytime environments. Here we test the hypothesis that opsin gene sequence plays a role in modifying firefly eye spectral sensitivity. We use genome and transcriptome sequencing in four firefly species, transcriptome sequencing in six additional species, and targeted gene sequencing in 28 other species to identify all opsin genes present in North American fireflies and to elucidate amino acid sites under positive selection. We also determine whether amino acid substitutions in opsins are linked to evolutionary changes in signal mode, signal color, and light environment. We find only two opsins, one long wavelength and one ultraviolet, in all firefly species and identify 25 candidate sites that may be involved in determining spectral sensitivity. In addition, we find elevated rates of evolution at transitions to diurnal activity, and changes in selective constraint on LW opsin associated with changes in light environment. Our results suggest that changes in eye spectral sensitivity are at least partially due to opsin sequence. Fireflies continue to be a promising system in which to investigate the evolution of signals, receptors, and signaling environments.

Oculogryphus chenghoiyanae sp. n. (Coleoptera, Lampyridae): a new ototretine firefly from Hong Kong with descriptions of its bioluminescent behavior and ultraviolet-induced fluorescence in females

“…Firefly males are likely to have ultraviolet vision (Martin et al 2015, Sander and Hall 2015). Oculogryphus species, however, are only active in the night when ultraviolet light is weak or totally absent, thus no UV-fluorescence by the females.…”

The impact of artificial light at night on nocturnal insects: A review and synthesis

“…To date, only UV‐ and long‐wavelength‐sensitive (UVS and LWS) opsin genes have been isolated from fireflies (Martin, Lord, Branham, & Bybee, ; Sander & Hall, ), although blue sensitivity has been observed in both North American and Japanese species using electroretinography (ERG) recordings (Eguchi, Nemoto, Meyer‐Rochow, & Ohba, ; Lall, Lord, & Ovid Trouth, ; Lall, Strother, Cronin, & Seliger, ). The peak sensitivity of the LWS photoreceptor generally corresponds to the peak wavelength of signals produced by that species (Sander & Hall, ). Signal reception is further tuned using filter pigments: In species that emit yellow bioluminescence, reddish filter pigments narrow visual sensitivity to the yellow region of the spectrum by blocking out green wavelengths (Booth, Stewart, & Osorio, ; Cronin, Järvilehto, Weckström, & Lall, ).…”

“…The superposition compound eyes of fireflies are finely attuned to conspecific signals: They are highly sensitive, but only to a narrow range of wavelengths. To date, only UV-and long-wavelength-sensitive (UVS and LWS) opsin genes have been isolated from fireflies (Martin, Lord, Branham, & Bybee, 2015;Sander & Hall, 2015), although blue sensitivity has been observed in both North American and Japanese species using electroretinography (ERG) recordings (Eguchi, Nemoto, Meyer-Rochow, & Ohba, 1984;Lall, Lord, & Ovid Trouth, 1982;Lall, Strother, Cronin, & Seliger, 1988). The peak sensitivity of the LWS photoreceptor generally corresponds to the peak wavelength of signals produced by that species (Sander & Hall, 2015).…”

Molecular variation across populations of a widespread North American firefly, Photinus pyralis, reveals that coding changes do not underlie flash color variation or associated visual sensitivity

“…To amplify each gene in its entirety, forward and reverse PCR primers were designed using Primer3 [80] from flanking sequences identified in P. pyralis transcriptome and genome sequences [15]. Both custom species-specific and previously published internal primers were then used to sequence each amplicon.…”