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How inversion variants can shape neural circuitry: Insights from the three-morph mating tactics of ruffs

Behavior polymorphisms underlying alternative mating tactics can evolve due to genetic inversions, especially when inversions capture sets of genes involved in hormonal regulation. In the three-morph system of the ruff (Calidris pugnax), two alternative morphs (Satellites and Faeders) with distinct...

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Autores principales: Loveland, Jasmine L., Giraldo-Deck, Lina M., Kelly, Aubrey M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9641025/
https://www.ncbi.nlm.nih.gov/pubmed/36388098
http://dx.doi.org/10.3389/fphys.2022.1011629
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author Loveland, Jasmine L.
Giraldo-Deck, Lina M.
Kelly, Aubrey M.
author_facet Loveland, Jasmine L.
Giraldo-Deck, Lina M.
Kelly, Aubrey M.
author_sort Loveland, Jasmine L.
collection PubMed
description Behavior polymorphisms underlying alternative mating tactics can evolve due to genetic inversions, especially when inversions capture sets of genes involved in hormonal regulation. In the three-morph system of the ruff (Calidris pugnax), two alternative morphs (Satellites and Faeders) with distinct behaviors and low circulating testosterone are genetically determined by an inverted region on an autosomal chromosome. Here, we discuss recent findings on the ruff and present novel insights into how an inversion that poses drastic constraints on testosterone production might lead to morph-specific differences in brain areas that regulate social behavior. A gene responsible for converting testosterone to androstenedione (HSD17B2) is located inside the inverted region and is a promising candidate. We identify a single missense mutation in the HSD17B2 gene of inverted alleles that is responsible for a 350–500% increase in testosterone to androstenedione conversion, when mutated in the human HSD17B2 protein. We discuss new evidence of morph differences in neural HSD17B2 expression in embryos and circulating androgens in sexually-immature juveniles. We suggest processes that shape morph differences in behavior likely begin early in ontogeny. We propose that the organization of behaviorally relevant neuron cell types that are canonically sexually dimorphic, such as subpopulations of aromatase and vasotocin neurons, should be particularly affected due to the life-long condition of low circulating testosterone in inversion morphs. We further emphasize how HSD17B2 catalytic activity extends beyond androgens, and includes estradiol oxidation into estrone and progesterone synthesis. Lastly, we underscore dimerization of HSD17B2 as an additional layer of complexity that merits consideration.
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spelling pubmed-96410252022-11-15 How inversion variants can shape neural circuitry: Insights from the three-morph mating tactics of ruffs Loveland, Jasmine L. Giraldo-Deck, Lina M. Kelly, Aubrey M. Front Physiol Physiology Behavior polymorphisms underlying alternative mating tactics can evolve due to genetic inversions, especially when inversions capture sets of genes involved in hormonal regulation. In the three-morph system of the ruff (Calidris pugnax), two alternative morphs (Satellites and Faeders) with distinct behaviors and low circulating testosterone are genetically determined by an inverted region on an autosomal chromosome. Here, we discuss recent findings on the ruff and present novel insights into how an inversion that poses drastic constraints on testosterone production might lead to morph-specific differences in brain areas that regulate social behavior. A gene responsible for converting testosterone to androstenedione (HSD17B2) is located inside the inverted region and is a promising candidate. We identify a single missense mutation in the HSD17B2 gene of inverted alleles that is responsible for a 350–500% increase in testosterone to androstenedione conversion, when mutated in the human HSD17B2 protein. We discuss new evidence of morph differences in neural HSD17B2 expression in embryos and circulating androgens in sexually-immature juveniles. We suggest processes that shape morph differences in behavior likely begin early in ontogeny. We propose that the organization of behaviorally relevant neuron cell types that are canonically sexually dimorphic, such as subpopulations of aromatase and vasotocin neurons, should be particularly affected due to the life-long condition of low circulating testosterone in inversion morphs. We further emphasize how HSD17B2 catalytic activity extends beyond androgens, and includes estradiol oxidation into estrone and progesterone synthesis. Lastly, we underscore dimerization of HSD17B2 as an additional layer of complexity that merits consideration. Frontiers Media S.A. 2022-10-25 /pmc/articles/PMC9641025/ /pubmed/36388098 http://dx.doi.org/10.3389/fphys.2022.1011629 Text en Copyright © 2022 Loveland, Giraldo-Deck and Kelly. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Physiology
Loveland, Jasmine L.
Giraldo-Deck, Lina M.
Kelly, Aubrey M.
How inversion variants can shape neural circuitry: Insights from the three-morph mating tactics of ruffs
title How inversion variants can shape neural circuitry: Insights from the three-morph mating tactics of ruffs
title_full How inversion variants can shape neural circuitry: Insights from the three-morph mating tactics of ruffs
title_fullStr How inversion variants can shape neural circuitry: Insights from the three-morph mating tactics of ruffs
title_full_unstemmed How inversion variants can shape neural circuitry: Insights from the three-morph mating tactics of ruffs
title_short How inversion variants can shape neural circuitry: Insights from the three-morph mating tactics of ruffs
title_sort how inversion variants can shape neural circuitry: insights from the three-morph mating tactics of ruffs
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9641025/
https://www.ncbi.nlm.nih.gov/pubmed/36388098
http://dx.doi.org/10.3389/fphys.2022.1011629
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