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1. Transcriptomic evidence for visual adaptation during the aquatic to terrestrial metamorphosis in leopard frogs

   https://doi.org/10.1186/s12915-022-01341-z  

   Schott, Ryan K. ; Bell, Rayna C. ; Loew, Ellis R. ; Thomas, Kate N. ; Gower, David J. ; Streicher, Jeffrey W. ; Fujita, Matthew K. ( June 2022 , BMC Biology)

   Differences in morphology, ecology, and behavior through ontogeny can result in opposing selective pressures at different life stages. Most animals, however, transition through two or more distinct phenotypic phases, which is hypothesized to allow each life stage to adapt more freely to its ecological niche. How this applies to sensory systems, and in particular how sensory systems adapt across life stages at the molecular level, is not well understood. Here, we used whole-eye transcriptomes to investigate differences in gene expression between tadpole and juvenile southern leopard frogs (Lithobates sphenocephalus), which rely on vision in aquatic and terrestrial light environments, respectively. Because visual physiology changes with light levels, we also tested the effect of light and dark exposure.

   We found 42% of genes were differentially expressed in the eyes of tadpoles versus juveniles and 5% for light/dark exposure. Analyses targeting a curated subset of visual genes revealed significant differential expression of genes that control aspects of visual function and development, including spectral sensitivity and lens composition. Finally, microspectrophotometry of photoreceptors confirmed shifts in spectral sensitivity predicted by the expression results, consistent with adaptation to distinct light environments.

   Overall, we identified extensive expression-level differences in the eyes of tadpoles and juveniles related to observed morphological and physiological changes through metamorphosis and corresponding adaptive shifts to improve vision in the distinct aquatic and terrestrial light environments these frogs inhabit during their life cycle. More broadly, these results suggest that decoupling of gene expression can mediate the opposing selection pressures experienced by organisms with complex life cycles that inhabit different environmental conditions throughout ontogeny.

    

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2. Comparisons of cell proliferation and cell death from tornaria larva to juvenile worm in the hemichordate Schizocardium californicum

   https://doi.org/10.1186/s13227-022-00198-1  

   Bump, Paul ; Khariton, Margarita ; Stubbert, Clover ; Moyen, Nicole E. ; Yan, Jia ; Wang, Bo ; Lowe, Christopher J. ( June 2022 , EvoDevo)

   There are a wide range of developmental strategies in animal phyla, but most insights into adult body plan formation come from direct-developing species. For indirect-developing species, there are distinct larval and adult body plans that are linked together by metamorphosis. Some outstanding questions in the development of indirect-developing organisms include the extent to which larval tissue undergoes cell death during the process of metamorphosis and when and where the tissue that will give rise to the adult originates. How do the processes of cell division and cell death redesign the body plans of indirect developers? In this study, we present patterns of cell proliferation and cell death during larval body plan development, metamorphosis, and adult body plan formation, in the hemichordateSchizocardium californium(Cameron and Perez in Zootaxa 3569:79–88, 2012) to answer these questions.

   We identified distinct patterns of cell proliferation between larval and adult body plan formation ofS. californicum. We found that some adult tissues proliferate during the late larval phase prior to the start of overt metamorphosis. In addition, using an irradiation and transcriptomic approach, we describe a genetic signature of proliferative cells that is shared across the life history states, as well as markers that are unique to larval or juvenile states. Finally, we observed that cell death is minimal in larval stages but begins with the onset of metamorphosis.

   Cell proliferation during the development ofS. californicumhas distinct patterns in the formation of larval and adult body plans. However, cell death is very limited in larvae and begins during the onset of metamorphosis and into early juvenile development in specific domains. The populations of cells that proliferated and gave rise to the larvae and juveniles have a genetic signature that suggested a heterogeneous pool of proliferative progenitors, rather than a set-aside population of pluripotent cells. Taken together, we propose that the gradual morphological transformation ofS. californicumis mirrored at the cellular level and may be more representative of the development strategies that characterize metamorphosis in many metazoan animals.

    

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3. Antennal transcriptome analysis reveals sensory receptors potentially associated with host detection in the livestock pest Lucilia cuprina

   https://doi.org/10.1186/s13071-024-06391-6  

   Wulff, Juan_P ; Hickner, Paul_V ; Watson, David_W ; Denning, Steven_S ; Belikoff, Esther_J ; Scott, Maxwell_J ( July 2024 , Parasites & Vectors)

   Lucilia cuprina(Wiedemann, 1830) (Diptera: Calliphoridae) is the main causative agent of flystrike of sheep in Australia and New Zealand. Female flies lay eggs in an open wound or natural orifice, and the developing larvae eat the host’s tissues, a condition called myiasis. To improve our understanding of host-seeking behavior, we quantified gene expression in male and female antennae based on their behavior.

   A spatial olfactometer was used to evaluate the olfactory response ofL. cuprinamated males and gravid females to fresh or rotting beef. Antennal RNA-Seq analysis was used to identify sensory receptors differentially expressed between groups.

   Lucilia cuprinafemales were more attracted to rotten compared to fresh beef (> fivefold increase). However, males and some females did not respond to either type of beef. RNA-Seq analysis was performed on antennae dissected from attracted females, non-attracted females and males. Transcripts encoding sensory receptors from 11 gene families were identified above a threshold (≥ 5 transcript per million) including 49 ATP-binding cassette transporters (ABCs), two ammonium transporters (AMTs), 37 odorant receptors (ORs), 16 ionotropic receptors (IRs), 5 gustatory receptors (GRs), 22 odorant-binding proteins (OBPs), 9 CD36-sensory neuron membrane proteins (CD36/SNMPs), 4 chemosensory proteins (CSPs), 4 myeloid lipid-recognition (ML) and Niemann-Pick C2 disease proteins (ML/NPC2), 2pickpocketreceptors (PPKs) and 3 transient receptor potential channels (TRPs). Differential expression analyses identified sex-biased sensory receptors.

   We identified sensory receptors that were differentially expressed between the antennae of both sexes and hence may be associated with host detection by female flies. The most promising for future investigations were as follows: an odorant receptor (LcupOR46) which is female-biased inL. cuprinaandCochliomyia hominivoraxCoquerel, 1858; an ABC transporter (ABC G23.1) that was the sole sensory receptor upregulated in the antennae of females attracted to rotting beef compared to non-attracted females; a female-biased ammonia transporter (AMT_Rh50), which was previously associated with ammonium detection inDrosophila melanogasterMeigen, 1830. This is the first report suggesting a possible role for ABC transporters inL. cuprinaolfaction and potentially in other insects.

    

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4. A learning experience elicits sex‐dependent neurogenomic responses in Bicyclus anynana butterflies

   https://doi.org/10.1111/mec.16920  

   Ernst, David A. ; Agcaoili, Gabrielle A. ; Merrill, Abbigail N. ; Westerman, Erica L. ( March 2023 , Molecular Ecology)

   Sexually dimorphic behaviour is pervasive across animals, with males and females exhibiting different mate selection, parental care, foraging, dispersal, and territorial strategies. However, the genetic underpinnings of sexually dimorphic behaviours are poorly understood. Here we investigate gene networks and expression patterns associated with sexually dimorphic imprinting‐like learning in the butterflyBicyclus anynana. In this species, both males and females learn visual preferences, but learn preferences for different traits and use different signals as salient, unconditioned cues. To identify genes and gene networks associated with this behaviour, we examined gene expression profiles of the brains and eyes of male and female butterflies immediately post training and compared them to the same tissues of naïve individuals. We found more differentially expressed genes and a greater number of associated gene networks in the eyes, indicating a role of the peripheral nervous system in visual imprinting‐like learning. Females had higher chemoreceptor expression levels than males, supporting the hypothesized sexual dimorphic use of chemical cues during the learning process. In addition, genes that influenceB. anynanawing patterns (sexual ornaments), such asinvected,spalt, andapterous, were also differentially expressed in the brain and eye, suggesting that these genes may influence both sexual ornaments and the preferences for these ornaments. Our results indicate dynamic and sex‐specific responses to social scenario in both the peripheral and central nervous systems and highlight the potential role of wing patterning genes in mate preference and learning across the Lepidoptera.

    

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5. Ocular lens morphology is influenced by ecology and metamorphosis in frogs and toads

   https://doi.org/10.1098/rspb.2022.0767  

   Mitra, Amartya T. ; Womack, Molly C. ; Gower, David J. ; Streicher, Jeffrey W. ; Clark, Brett ; Bell, Rayna C. ; Schott, Ryan K. ; Fujita, Matthew K. ; Thomas, Kate N. ( November 2022 , Proceedings of the Royal Society B: Biological Sciences)

   The shape and relative size of an ocular lens affect the focal length of the eye, with consequences for visual acuity and sensitivity. Lenses are typically spherical in aquatic animals with camera-type eyes and axially flattened in terrestrial species to facilitate vision in optical media with different refractive indices. Frogs and toads (Amphibia: Anura) are ecologically diverse, with many species shifting from aquatic to terrestrial ecologies during metamorphosis. We quantified lens shape and relative size using 179 micro X-ray computed tomography scans of 126 biphasic anuran species and tested for correlations with life stage, environmental transitions, adult habits and adult activity patterns. Across broad phylogenetic diversity, tadpole lenses are more spherical than those of adults. Biphasic species with aquatic larvae and terrestrial adults typically undergo ontogenetic changes in lens shape, whereas species that remain aquatic as adults tend to retain more spherical lenses after metamorphosis. Further, adult lens shape is influenced by adult habit; notably, fossorial adults tend to retain spherical lenses following metamorphosis. Finally, lens size relative to eye size is smaller in aquatic and semiaquatic species than other adult ecologies. Our study demonstrates how ecology shapes visual systems, and the power of non-invasive imaging of museum specimens for studying sensory evolution. 

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