Counter-gradient variation and the expensive tissue hypothesis explain parallel brain size reductions at high elevation in cricetid and murid rodents
Abstract To better understand functional morphological adaptations to high elevation (> 3000 m above sea level) life in both North American and African mountain-associated rodents, we used microCT scanning to acquire 3D images and a 3D morphometric approach to calculate endocranial volumes and sk...
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Nature Portfolio
2023-04-01
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| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-023-32498-4 |
| _version_ | 1797850078019321856 |
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| author | Aluwani Nengovhela Catherine M. Ivy Graham R. Scott Christiane Denys Peter J. Taylor |
| author_facet | Aluwani Nengovhela Catherine M. Ivy Graham R. Scott Christiane Denys Peter J. Taylor |
| author_sort | Aluwani Nengovhela |
| collection | DOAJ |
| description | Abstract To better understand functional morphological adaptations to high elevation (> 3000 m above sea level) life in both North American and African mountain-associated rodents, we used microCT scanning to acquire 3D images and a 3D morphometric approach to calculate endocranial volumes and skull lengths. This was done on 113 crania of low-elevation and high-elevation populations in species of North American cricetid mice (two Peromyscus species, n = 53), and African murid rodents of two tribes, Otomyini (five species, n = 49) and Praomyini (four species, n = 11). We tested two distinct hypotheses for how endocranial volume might vary in high-elevation populations: the expensive tissue hypothesis, which predicts that brain and endocranial volumes will be reduced to lessen the costs of growing and maintaining a large brain; and the brain-swelling hypothesis, which predicts that endocranial volumes will be increased either as a direct phenotypic effect or as an adaptation to accommodate brain swelling and thus minimize pathological symptoms of altitude sickness. After correcting for general allometric variation in cranial size, we found that in both North American Peromyscus mice and African laminate-toothed (Otomys) rats, highland rodents had smaller endocranial volumes than lower-elevation rodents, consistent with the expensive tissue hypothesis. In the former group, Peromyscus mice, crania were obtained not just from wild-caught mice from high and low elevations but also from those bred in common-garden laboratory conditions from parents caught from either high or low elevations. Our results in these mice showed that brain size responses to elevation might have a strong genetic basis, which counters an opposite but weaker environmental effect on brain volume. These results potentially suggest that selection may act to reduce brain volume across small mammals at high elevations but further experiments are needed to assess the generality of this conclusion and the nature of underlying mechanisms. |
| first_indexed | 2024-04-09T18:54:33Z |
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| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-04-09T18:54:33Z |
| publishDate | 2023-04-01 |
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| spelling | doaj.art-133d5850e8cb4d1b97e46926b9fb931b2023-04-09T11:14:57ZengNature PortfolioScientific Reports2045-23222023-04-0113111110.1038/s41598-023-32498-4Counter-gradient variation and the expensive tissue hypothesis explain parallel brain size reductions at high elevation in cricetid and murid rodentsAluwani Nengovhela0Catherine M. Ivy1Graham R. Scott2Christiane Denys3Peter J. Taylor4Department of Mammalogy, National MuseumDepartment of Biology, McMaster UniversityDepartment of Biology, McMaster UniversityInstitut de Systématique, Evolution, Biodiversité (ISYEB), Muséum National d’Histoire Naturelle, CNRS, Sorbonne Université, EPHE, Université des AntillesDepartment of Zoology, School of Natural and Mathematical Sciences, University of VendaAbstract To better understand functional morphological adaptations to high elevation (> 3000 m above sea level) life in both North American and African mountain-associated rodents, we used microCT scanning to acquire 3D images and a 3D morphometric approach to calculate endocranial volumes and skull lengths. This was done on 113 crania of low-elevation and high-elevation populations in species of North American cricetid mice (two Peromyscus species, n = 53), and African murid rodents of two tribes, Otomyini (five species, n = 49) and Praomyini (four species, n = 11). We tested two distinct hypotheses for how endocranial volume might vary in high-elevation populations: the expensive tissue hypothesis, which predicts that brain and endocranial volumes will be reduced to lessen the costs of growing and maintaining a large brain; and the brain-swelling hypothesis, which predicts that endocranial volumes will be increased either as a direct phenotypic effect or as an adaptation to accommodate brain swelling and thus minimize pathological symptoms of altitude sickness. After correcting for general allometric variation in cranial size, we found that in both North American Peromyscus mice and African laminate-toothed (Otomys) rats, highland rodents had smaller endocranial volumes than lower-elevation rodents, consistent with the expensive tissue hypothesis. In the former group, Peromyscus mice, crania were obtained not just from wild-caught mice from high and low elevations but also from those bred in common-garden laboratory conditions from parents caught from either high or low elevations. Our results in these mice showed that brain size responses to elevation might have a strong genetic basis, which counters an opposite but weaker environmental effect on brain volume. These results potentially suggest that selection may act to reduce brain volume across small mammals at high elevations but further experiments are needed to assess the generality of this conclusion and the nature of underlying mechanisms.https://doi.org/10.1038/s41598-023-32498-4 |
| spellingShingle | Aluwani Nengovhela Catherine M. Ivy Graham R. Scott Christiane Denys Peter J. Taylor Counter-gradient variation and the expensive tissue hypothesis explain parallel brain size reductions at high elevation in cricetid and murid rodents Scientific Reports |
| title | Counter-gradient variation and the expensive tissue hypothesis explain parallel brain size reductions at high elevation in cricetid and murid rodents |
| title_full | Counter-gradient variation and the expensive tissue hypothesis explain parallel brain size reductions at high elevation in cricetid and murid rodents |
| title_fullStr | Counter-gradient variation and the expensive tissue hypothesis explain parallel brain size reductions at high elevation in cricetid and murid rodents |
| title_full_unstemmed | Counter-gradient variation and the expensive tissue hypothesis explain parallel brain size reductions at high elevation in cricetid and murid rodents |
| title_short | Counter-gradient variation and the expensive tissue hypothesis explain parallel brain size reductions at high elevation in cricetid and murid rodents |
| title_sort | counter gradient variation and the expensive tissue hypothesis explain parallel brain size reductions at high elevation in cricetid and murid rodents |
| url | https://doi.org/10.1038/s41598-023-32498-4 |
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