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1. 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)

   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 mouthbroodingmore »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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2. Endocrine Modulation of Sending and Receiving Signals in Context-Dependent Social Communication

   https://doi.org/10.1093/icb/icab074  

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

   Abstract Animal communication requires senders to transmit signals through the environment to conspecific receivers, which then leads to context-dependent behavioral decisions. Sending and receiving sensory information in social contexts, however, can be dramatically influenced by an individual’s internal state, particularly in species that cycle in and out of breeding or other physiological condition like nutritional state or social status. Modulatory substances like steroids, peptides, and biogenic amines can influence both the substrates used for sending social signals (e.g., motivation centers, sensorimotor pathways, and muscles) as well as the peripheral sensory organs and central neural circuitry involved in the reception of this information and subsequent execution of behavioral responses. This issue highlights research from neuroethologists on the topic of modulation of sending and receiving social signals and demonstrates that it can occur in both males and females, in different senses at both peripheral sensory organs and the brain, at different levels of biological organization, on different temporal scales, in various social contexts, and across many diverse vertebrate taxa. Modifying a signal produced by a sender or how that signal is perceived in a receiver provides flexibility in communication and has broad implications for influencing social decisions like mate choice, which ultimatelymore »affects reproductive fitness and species persistence. This phenomenon of modulators and internal physiological state impacting communication abilities is likely more widespread than currently realized and we hope this issue inspires others working on diverse systems to examine this topic from different perspectives. An integrative and comparative approach will advance discovery in this field and is needed to better understand how endocrine modulation contributes to sexual selection and the evolution of animal communication in general.« less
3. Widespread Gene Expression Divergence in Butterfly Sensory Tissues Plays a Fundamental Role During Reproductive Isolation and Speciation

   https://doi.org/10.1093/molbev/msac225  

   Wu, Ningning ; Evans, Elizabeth ; van Schooten, Bas ; Meléndez-Rosa, Jesyka ; Ortiz, Yadira ; Planas Soto-Navarro, Silvia M ; Van Belleghem, Steven M ; Counterman, Brian A ; Papa, Riccardo ; Zhang, Wei ( November 2022 , Molecular Biology and Evolution)

   Wei, Fuwen (Ed.)

   Abstract Neotropical Heliconius butterflies are well known for their intricate behaviors and multiple instances of incipient speciation. Chemosensing plays a fundamental role in the life history of these groups of butterflies and in the establishment of reproductive isolation. However, chemical communication involves synergistic sensory and accessory functions, and it remains challenging to investigate the molecular mechanisms underlying behavioral differences. Here, we examine the gene expression profiles and genomic divergence of three sensory tissues (antennae, legs, and mouthparts) between sexes (females and males) and life stages (different adult stages) in two hybridizing butterflies, Heliconius melpomene and Heliconius cydno. By integrating comparative transcriptomic and population genomic approaches, we found evidence of widespread gene expression divergence, supporting a crucial role of sensory tissues in the establishment of species barriers. We also show that sensory diversification increases in a manner consistent with evolutionary divergence based on comparison with the more distantly related species Heliconius charithonia. The findings of our study strongly support the unique chemosensory function of antennae in all three species, the importance of the Z chromosome in interspecific divergence, and the nonnegligible role of nonchemosensory genes in the divergence of chemosensory tissues. Collectively, our results provide a genome-wide illustration of diversification inmore »the chemosensory system under incomplete reproductive isolation, revealing strong molecular separation in the early stage of speciation. Here, we provide a unique perspective and relevant view of the genetic architecture (sensory and accessory functions) of chemosensing beyond the classic chemosensory gene families, leading to a better understanding of the magnitude and complexity of molecular changes in sensory tissues that contribute to the establishment of reproductive isolation and speciation.« less
4. 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 undermore »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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5. Robustness in action: Leg loss does not affect mating success in male harvestmen

   https://doi.org/10.1007/s00265-022-03127-3  

   Escalante, Ignacio ; Elias, Damian O. ( January 2022 , Behavioral Ecology and Sociobiology)

   Defensive strategies, like other life-history traits favored by natural selection, may pose constraints on reproduction. A common anti-predator defense strategy that increases immediate survival is autotomy—the voluntary release of body parts. This type of morphological damage is considered to impose future costs for reproduction and fitness. We tested an alternative hypothesis that animals are robust (able to withstand and overcome perturbations) to this type of damage and do not experience any fitness costs in reproductive contexts. We explored the effects of experimental leg loss on the reproductive behavior of one species of NeotropicalPrionostemmaharvestmen. These arachnids undergo autotomy frequently, do not regenerate legs, and their courtship and mating necessitate the use of legs. We assessed the effect of losing different types of legs (locomotor or sensory) on courtship behavior and mating success in males. We found no differences in the mating success or in any measured aspect of reproductive behavior between eight-legged males and males that experienced loss of legs of any type. Additionally, we found that morphological traits related to body size did not predict mating success. Overall, our experimental findings support the null hypothesis that harvestmen are robust to the consequences of morphological damage and natural selection favors strategiesmore »that increase robustness.

   In order to survive encounters with predators, animals have evolved many defensive strategies. Some of those behaviors, however, can come with a cost to their overall body condition. For example, some animals can voluntarily lose body parts (tails, legs, etc.) to escape. This process can then affect many aspects of an animal’s life, including reproduction. In a group of harvestmen (daddy long-legs) from Costa Rica, we tested the hypothesis that males are robust to the potential consequences of losing legs, and will not experience costs. We found that males that lost either legs used for locomotion or for sensory perception reproduced in the same way as animals with all of their legs. Consequently, we demonstrate that these arachnids are able to withstand the loss of legs with no effects on reproduction.

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