Beauty in the eye of the beholder: the two blue opsins of lycaenid butterflies and the opsin gene-driven evolution of sexually dimorphic eyes

Abstract

SUMMARY Although previous investigations have shown that wing coloration is an important component of social signaling in butterflies, the contribution of opsin evolution to sexual wing color dichromatism and interspecific divergence remains largely unexplored. Here we report that the butterfly Lycaena rubidus has evolved sexually dimorphic eyes due to changes in the regulation of opsin expression patterns to match the contrasting life histories of males and females. The L. rubidus eye contains four visual pigments with peak sensitivities in the ultraviolet (UV;λ max=360 nm), blue (B; λmax=437 nm and 500 nm, respectively) and long (LW; λmax=568 nm) wavelength range. By combining in situ hybridization of cloned opsinencoding cDNAs with epi-microspectrophotometry, we found that all four opsin mRNAs and visual pigments are expressed in the eyes in a sex-specific manner. The male dorsal eye, which contains only UV and B (λmax=437 nm)visual pigments, indeed expresses two short wavelength opsin mRNAs, UVRh and BRh1. The female dorsal eye, which also has the UV and B (λmax=437 nm) visual pigments, also contains the LW visual pigment, and likewise expresses UVRh, BRh1 and LWRh mRNAs. Unexpectedly, in the female dorsal eye, we also found BRh1 co-expressed with LWRh in the R3-8 photoreceptor cells. The ventral eye of both sexes, on the other hand, contains all four visual pigments and expresses all four opsin mRNAs in a non-overlapping fashion. Surprisingly, we found that the 500 nm visual pigment is encoded by a duplicate blue opsin gene, BRh2. Further, using molecular phylogenetic methods we trace this novel blue opsin gene to a duplication event at the base of the Polyommatine+Thecline+Lycaenine radiation. The blue opsin gene duplication may help explain the blueness of blue lycaenid butterflies.

Absence of eye shine and tapetum in the heterogeneous eye ofAnthocharisbutterflies (Pieridae)

“…The retina of some nymphaline butterflies is probably organized in a very similar way (Briscoe and Bernard, 2005). Yet, other nymphalids have clearly recruited red photoreceptor screening pigments that act as red filters (Stavenga et al, 2001;Stavenga, 2002a;Stavenga, 2002b;Sauman et al, 2005;Zaccardi et al, 2006), and the same holds for papilionids (Arikawa and Stavenga, 1997;Arikawa, 2003) and lycaenids (Arikawa and Stavenga, 1997;Stavenga, 2002a;Sison-Mangus et al, 2006). Furthermore, detailed molecular biological analyses revealed that in the latter case the short-wavelength receptors diversified to such an extent that no less than six ommatidial types exist .…”

Opsin expression, physiological characterization and identification of photoreceptor cells in the dorsal rim area and main retina of the desert locust,Schistocerca gregaria

“…However, in some other Lepidoptera (e.g. Sison-Mangus et al, 2006;Awata et al, 2010), Diptera (e.g. Hu et al, 2011) and the two-spotted cricket (Henze et al, 2012), a dorsal-ventral gradient or regionalization was found with higher expression of longwavelength opsins in ventral eye regions.…”

Sexual dimorphism in the compound eye of Heliconius erato: a nymphalid butterfly with at least five spectral classes of photoreceptor

“…Butterflies are known for the diversity in their photoreceptor spectral sensitivities (Arikawa et al, 1987(Arikawa et al, , 2005Sison-Mangus et al, 2006;Briscoe, 2008;Ogawa et al, 2012). In several butterfly families, this diversity has been achieved by independent increases in the number of spectrally distinct photoreceptors in the adult compound eye, via three mechanisms.…”

“…At least one species in the Riodinidae has duplicated a LW opsin (Frentiu et al, 2007). B opsin gene duplications have resulted in spectrally distinct receptors in the range 435-500 nm in the family Lycaenidae (Sison-Mangus et al, 2006, 2008 and independently in Pieridae. In addition, both Pieris and Colias (Pieridae) have complex patterns of lateral filtering pigments, which in Colias erate results in nine spectral classes of photoreceptor, including multiple red-sensitive cells (Qiu et al, 2002;Qiu and Arikawa, 2003;Arikawa et al, 2005;Awata et al, 2009;Ogawa et al, 2012Ogawa et al, , 2013.…”