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1. Diversity in olfactory receptor repertoires is associated with dietary specialization in a genus of frugivorous bat

   https://doi.org/10.1093/g3journal/jkab260  

   Yohe, Laurel R ; Leiser-Miller, Leith B ; Kaliszewska, Zofia A ; Donat, Paul ; Santana, Sharlene E ; Dávalos, Liliana M ( July 2021 , G3 Genes|Genomes|Genetics)

   null (Ed.)

   Abstract Mammalian olfactory receptor genes (ORs) are a diverse family of genes encoding proteins that directly interact with environmental chemical cues. ORs evolve via gene duplication in a birth-death fashion, neofunctionalizing and pseudogenizing over time. Olfaction is a primary sense used for food detection in plant-visiting bats, but the relationship between dietary specialization and OR repertoire diversity is unclear. Within neotropical Leaf-nosed bats (Phyllostomidae), many lineages are plant specialists, and some have a distinct OR repertoire compared to insectivorous species. Yet, whether specialization on particular plant genera is associated with the evolution of specialized, less diverse OR repertoires has never been tested. Using targeted sequence capture, we sequenced the OR repertoires of three sympatric species of short-tailed fruit bats (Carollia), which vary in their degree of specialization on the fruits of Piper plants. We characterized orthologous vs duplicated receptors among Carollia species, and explored the diversity and redundancy of the receptor gene repertoire. At the species level, the most dedicated Piper specialist, Carollia castanea, had lower OR diversity compared to the two generalists (C. sowelli and C. perspicillata), but we discovered a few unique sets of ORs within C. castanea with high redundancy of similar gene duplicates. These unique receptors potentially enable C. castanea to detect Piper fruit odorants better than its two congeners. Carollia perspicillata, the species with the most generalist diet, had a higher diversity of intact receptors, suggesting the ability to detect a wider range of odorant molecules. Variation among ORs may be a factor in the coexistence of these sympatric species, facilitating the exploitation of different plant resources. Our study sheds light on how gene duplication and changes in OR diversity may play a role in dietary adaptations and underlie ecological interactions between bats and plants. 

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2. Comparative growth in the olfactory system of the developing chick with considerations for evolutionary studies

   https://doi.org/10.1111/joa.13197  

   Hogan, Aneila V. C. ; Watanabe, Akinobu ; Balanoff, Amy M. ; Bever, Gabriel S. ( April 2020 , Journal of Anatomy)

   Despite the long‐held assumption that olfaction plays a relatively minor role in the behavioral ecology of birds, crown‐group avians exhibit marked phylogenetic variation in the size and form of the olfactory apparatus. As part of a larger effort to better understand the role of olfaction and olfactory tissues in the evolution and development of the avian skull, we present the first quantitative analysis of ontogenetic scaling between olfactory features [olfactory bulbs (OBs) and olfactory turbinates] and neighboring structures (cerebrum, total brain, respiratory turbinates) based on the model organismGallus gallus. The OB develops under the predictions of a concerted evolutionary model with rapid early growth that is quickly overcome by the longer, sustained growth of the larger cerebrum. A similar pattern is found in the nasal cavity where the morphologically simple (non‐scrolled) olfactory turbinates appear and mature early, with extended growth characterizing the larger and scrolled respiratory turbinates. Pairwise regressions largely recover allometric relationships among the examined structures, with a notable exception being the isometric trajectory of the OB and olfactory turbinate. Their parallel growth suggests a unique regulatory pathway that is likely driven by the morphogenesis of the olfactory nerve, which serves as a structural bridge between the two features. Still, isometry was not necessarily expected given that the olfactory epithelium covers more than just the turbinate. These data illuminate a number of evolutionary hypotheses that, moving forward, should inform tradeoffs and constraints between the olfactory and neighboring systems in the avian head.

    

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3. What is that smell? Hummingbirds avoid foraging on resources with defensive insect compounds

   https://doi.org/10.1007/s00265-021-03067-4  

   Kim, Ashley Y. ; Rankin, David T. ; Rankin, Erin E. Wilson ( September 2021 , Behavioral Ecology and Sociobiology)

   Hummingbirds utilize visual cues to locate flowers, but little is known about the role olfaction plays in nectar foraging despite observations that hummingbirds avoid resources occupied by certain insects. We investigated the behavioral responses of both wild and captive hummingbirds to olfactory cues of hymenopteran floral visitors, including native wood ants (Formica francoeuri), invasive Argentine ants (Linepithema humile), and European honeybees (Apis mellifera). We demonstrate for the first time that hummingbirds use olfaction to make foraging decisions when presented with insect-derived chemical cues under field and aviary conditions. Both wild and captive hummingbirds avoided foraging on feeders with defensive chemicals ofF. francoeuriand aggregation pheromones ofL. humile, but showed no response to honeybee cuticular hydrocarbons. Our experiments demonstrate the importance of olfaction in shaping hummingbird foraging decisions.

   Recent reviews reveal that avian olfaction is not just limited to vultures and a few taxa. We demonstrate that a very charismatic group, hummingbirds, avoid defensive and aggregatory chemical cues from insects present at nectar resources. Olfactory cues can provide critical information about the presence and potential threat of insect floral visitors. This study raises new questions about the underrated importance of olfaction in avian foraging and specifically, hummingbird foraging.

    

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4. Ecological constraints on highly evolvable olfactory receptor genes and morphology in neotropical bats

   https://doi.org/10.1111/evo.14591  

   Yohe, Laurel R. ; Fabbri ; Lee, Daniela ; Davies, Kalina T.J. ; Yohe, Thomas P. ; Sánchez, Miluska K.R. ; Rengifo, Edgardo M. ; Hall, Ronald ; Mutumi, Gregory ; Hedrick, Brandon P. ; et al ( January 2022 , Evolution)

   While evolvability of genes and traits may promote specialization during species diversification, how ecology subsequently restricts such variation remains unclear. Chemosensation requires animals to decipher a complex chemical background to locate fitness-related resources, and thus the underlying genomic architecture and morphology must cope with constant exposure to a changing odorant landscape; detecting adaptation amidst extensive chemosensory diversity is an open challenge. In phyllostomid bats, an ecologically diverse clade that evolved plant-visiting from an insectivorous ancestor, the evolution of novel food detection mechanisms is suggested to be a key innovation, as plant-visiting species rely strongly on olfaction, supplementarily using echolocation. If this is true, exceptional variation in underlying olfactory genes and phenotypes may have preceded dietary diversification. We compared olfactory receptor (OR) genes sequenced from olfactory epithelium transcriptomes and olfactory epithelium surface area of bats with differing diets. Surprisingly, although OR evolution rates were quite variable and generally high, they are largely independent of diet. Olfactory epithelial surface area, however, is relatively larger in plant-visiting bats and there is an inverse relationship between OR evolution rates and surface area. Relatively larger surface areas suggest greater reliance on olfactory detection and stronger constraint on maintaining an already diverse OR repertoire. Instead of the typical case in which specialization and elaboration are coupled with rapid diversification of associated genes, here the relevant genes are already evolving so quickly that increased reliance on smell has led to stabilizing selection, presumably to maintain the ability to consistently discriminate among specific odorants — a potential ecological constraint on sensory evolution. 

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5. On the evolution of mimicry in avian nestlings

   https://doi.org/10.1002/ece3.8842  

   Londoño, Gustavo A. ; Sandoval‐H, Juliana ; Sallam, Mohamed F. ; Allen, Julie M. ( April 2022 , Ecology and Evolution)

   Batesian mimicry (BM), where a nontoxic species resembles a toxic species with aposematic coloring, has been recently described for a Neotropical species of the suboscine passerine (Laniocera hypopyrra). Understanding the order and series in which these characteristics evolved is unknown and requires character information from closely related taxa. Here, we trace the origin of mimetic traits and how they evolved by examining antipredator characteristics using images and other field‐collected trait data from nest and nestlings along with data available in the literature for the Laniisominae clade and closely related taxa. We found that morphological modifications of the downy feathers appeared first in the broader clade leading to the Laniisominae clade followed by further morphological and behavioral characteristics within the Laniisominae clade leading to the full BM. Images of nestlings in the Laniisominae and closely related clades demonstrated the extent of antipredator and camouflage characteristics. We found a complex set of behavioral and morphological traits in this clade for reducing predation from hiding to camouflage to mimicry. We further propose the evolution of two distinctive mimicry strategies in the Laniisominae clade: (1) Batesian Mimicry, as described above and (2) Masquerade, resemblance to inedible objects commonly found in their local environment. This complex set of antipredator traits shed light on the diversity of antipredator characteristics in avian nestlings, particularly in neotropical areas where the avian diversity is highest. Unfortunately, there are hundreds of species in the neotropics that lack basic natural history information on nesting traits, and therefore, we are likely missing critical information on the diversity of antipredator characteristics across avian nestlings.

    

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