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1. Modular genetic control of social status in a cichlid fish

   https://doi.org/10.1073/pnas.2008925117  

   Alward, Beau A.; Laud, Vibhav A.; Skalnik, Christopher J.; York, Ryan A.; Juntti, Scott A.; Fernald, Russell D. (October 2020, Proceedings of the National Academy of Sciences)

   Social hierarchies are ubiquitous in social species and profoundly influence physiology and behavior. Androgens like testosterone have been strongly linked to social status, yet the molecular mechanisms regulating social status are not known. The African cichlid fishAstatotilapia burtoniis a powerful model species for elucidating the role of androgens in social status given their rich social hierarchy and genetic tractability. DominantA. burtonimales possess large testes and bright coloration and perform aggressive and reproductive behaviors while nondominant males do not. Social status inA. burtoniis in flux, however, as males alter their status depending on the social environment. Due to a teleost-specific whole-genome duplication,A. burtonipossess two androgen receptor (AR) paralogs,ARαandARβ, providing a unique opportunity to disentangle the role of gene duplication in the evolution of social systems. Here, we used CRISPR/Cas9 gene editing to generate AR mutantA. burtoniand performed a suite of experiments to interrogate the mechanistic basis of social dominance. We find thatARβ,but notARα, is required for testes growth and bright coloration, whileARα, but notARβ, is required for the performance of reproductive behavior and aggressive displays. Both receptors are required to reduce flees from females and either AR is sufficient for attacking males. Thus, social status inA. burtoniis inordinately dissociable and under the modular control of two AR paralogs. This type of nonredundancy may be important in facilitating social plasticity inA. burtoniand other species whose social status relies on social experience. 

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2. Intra‐population variation in male nuptial coloration and diet across anthropogenically altered visual microhabitats in an African cichlid

   https://doi.org/10.1111/jzo.12996  

   Atkinson, T. L.; Gray, S. M. (June 2022, Journal of Zoology)

   Abstract Human activities are altering natural ecosystems, leading to widespread environmental change that can vary across spatiotemporal scales, thus creating dynamic, novel conditions at both large and small scales. In highly disturbed aquatic systems, elevated turbidity is one common stressor that alters the sensory environment of fishes and can disrupt communication, including mate choice, driving population‐level shifts in visual communication traits such as nuptial coloration. At a smaller, within‐population scale, we can expect similar adaptive divergence to a heterogeneous visual landscape. Using the cichlid fish,Pseudocrenilabrus multicolor,we investigated within‐population variation in diet and nuptial coloration by sampling fish from microhabitats within a relatively small site (~0.14 km²). These visual microhabitats are affected by different types of human disturbance at a very small scale leading to significant differences in water clarity (i.e. turbidity). We used three, non‐mutually exclusive working hypotheses to test if (1) males in low turbidity invest more in carotenoid‐based coloration (economy of pigments hypothesis), (2) fish from low‐turbidity sites eat more carotenoid‐rich foods (diet hypothesis), and (3) fish are habitat matching. Stomach content analyses revealed relatively high overlap in diet across microhabitats; however, fish from stations with the lowest turbidity consumed relatively more plant material (high in carotenoid content) than fish captured at high‐turbidity stations. Males from clearer waters displayed significantly more carotenoid‐based, red and yellow coloration than fish found in microhabitats with higher turbidity, similar to between‐population color variation in this species. Furthermore, larger fish displayed more carotenoid coloration overall, but there was no difference in mean male size among microhabitats suggesting that fish were not sorting into microhabitats. Our results suggest that within‐population variation in nuptial coloration could be associated with microhabitat heterogeneity in the visual landscape driven by turbidity, a diet with more carotenoid‐rich prey items, or a combination of both. 

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3. Transcriptomic analyses during development reveal mechanisms of integument structuring and color production

   https://doi.org/10.1007/s10682-023-10256-2  

   Stuckert, Adam M.; Freeborn, Layla; Howell, Kimberly A.; Yang, Yusan; Nielsen, Rasmus; Richards-Zawacki, Corinne; MacManes, Matthew D. (September 2023, Evolutionary Ecology)

   Abstract Skin coloration and patterning play a key role in animal survival and reproduction. As a result, color phenotypes have generated intense research interest. In aposematic species, color phenotypes can be important in avoiding predation and in mate choice. However, we still know little about the underlying genetic mechanisms of color production, particularly outside of a few model organisms. Here we seek to understand the genetic mechanisms underlying the production of different colors and how these undergo shifting expression patterns throughout development. To answer this, we examine gene expression of two different color patches(yellow and green) in a developmental time series from young tadpoles through adults in the poison frogOophaga pumilio.We identified six genes that were differentially expressed between color patches in every developmental stage (casq1, hand2, myh8, prva, tbx3,andzic1).Of these,hand2, myh8, tbx3,andzic1have either been identified or implicated as important in coloration in other taxa.Casq1andprvabuffer Ca²⁺and are a Ca²⁺transporter, respectively, and may play a role in preventing autotoxicity to pumiliotoxins, which inhibit Ca²⁺-ATPase activity. We identify further candidate genes (e.g.,adh, aldh1a2, asip, lef1, mc1r, tyr, tyrp1, xdh), and identify a suite of hub genes that likely play a key role in integumental reorganization during development (e.g., collagen type I–IV genes, lysyl oxidases) which may also affect coloration via structural organization of chromatophores that contribute to color and pattern. Overall, we identify the putative role of a suite of candidate genes in the production of different color types in a polytypic, aposematic species. 

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4. Opsin Expression Varies with Reproductive State in the Cichlid Fish Astatotilapia burtoni

   https://doi.org/10.1093/icb/icab058  

   Butler, Julie M.; Maruska, Karen P. (October 2021, Integrative and Comparative Biology)

   Synopsis Animals use visual communication to convey crucial information about their identity, reproductive status, and sex. Plasticity in the auditory and olfactory systems has been well-documented, however, fewer studies have tested for plasticity in the visual system, a surprising detail since courtship and mate choice are largely dependent on visual signals across taxa. We previously found reproductive state-dependent plasticity in the eye of the highly social cichlid fish Astatotilapia burtoni. Male A. burtoni increase their courtship, including multicomponent visual displays, when around ovulated females, and ovulated females are more responsive to male visual courtship displays than non-ovulated females. Based on this, we hypothesized that ovulation status impacts visual capabilities in A. burtoni females. Using electroretinograms, we found that ovulated females had greater visual sensitivity at wavelengths corresponding to male courtship coloration compared with non-reproductively-receptive females. In addition, ovulated females had higher neural activation in the retina and higher mRNA expression levels of neuromodulatory receptors (e.g., sex-steroids; gonadotropins) in the eye than non-ovulated females. Here, we add to this body of work by testing the hypothesis that cone opsin expression changes with female reproductive state. Ovulated females had higher expression of short wavelength sensitive opsins (sws1, sws2a, sws2b) compared with mouthbrooding females. Further, expression of sws2a, the most abundant opsin in the A. burtoni eye, positively correlated with levels of circulating 11-ketotestosterone and estradiol and estrogen, androgen, and gonadotropin system receptor expression in the eye in females. These data indicate that reproductive state-dependent plasticity also occurs at the level of photoreceptors, not just through modulation of visual signals at downstream retinal layers. Collectively, these data provide crucial evidence linking endocrine modulation of visual plasticity to mate choice behaviors in females. 

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5. True UV color vision in a female butterfly with two UV opsins

   https://doi.org/10.1242/jeb.242802  

   Finkbeiner, Susan D.; Briscoe, Adriana D. (September 2021, Journal of Experimental Biology)

   ABSTRACT In true color vision, animals discriminate between light wavelengths, regardless of intensity, using at least two photoreceptors with different spectral sensitivity peaks. Heliconius butterflies have duplicate UV opsin genes, which encode ultraviolet and violet photoreceptors, respectively. In Heliconius erato, only females express the ultraviolet photoreceptor, suggesting females (but not males) can discriminate between UV wavelengths. We tested the ability of H. erato, and two species lacking the violet receptor, Heliconius melpomene and Eueides isabella, to discriminate between 380 and 390 nm, and between 400 and 436 nm, after being trained to associate each stimulus with a sugar reward. We found that only H. erato females have color vision in the UV range. Across species, both sexes show color vision in the blue range. Models of H. erato color vision suggest that females have an advantage over males in discriminating the inner UV-yellow corollas of Psiguria flowers from their outer orange petals. Moreover, previous models ( McCulloch et al., 2017) suggested that H. erato males have an advantage over females in discriminating Heliconius 3-hydroxykynurenine (3-OHK) yellow wing coloration from non-3-OHK yellow wing coloration found in other heliconiines. These results provide some of the first behavioral evidence for female H. erato UV color discrimination in the context of foraging, lending support to the hypothesis ( Briscoe et al., 2010) that the duplicated UV opsin genes function together in UV color vision. Taken together, the sexually dimorphic visual system of H. erato appears to have been shaped by both sexual selection and sex-specific natural selection. 

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