Adaptation in brain structure and respiratory and olfactory structures across environmental gradients in African and North American muroid rodents.

Morphometric studies of 3D micro CT-scanned images can provide insights into the evolution of the brain and sensory structures but such data are still scarce for the most diverse mammalian order of rodents. From reviewed and new data, we tested for convergence to extreme aridity and high elevation in the sensory and brain morphology of rodents, from morphometric data from micro-CT X-ray scans of 174 crania of 16 species of three distantly related African murid (soft-furred mice, Praomyini, laminate-toothed rats, Otomyini, and gerbils, Gerbillinae) clades and one North American cricetid (deer mice and white-footed mice, Peromyscus) clade. Recent studies demonstrated convergent evolution acting on the oval window area of the cochlea (enlarged in extremely arid-adapted species of Otomyini and Gerbillinae) and on endocranial volume (reduced in high elevation taxa of Otomyini and Peromyscus). However, contrary to our predictions, we did not find evidence of convergence in brain structure to aridity, or in the olfactory/respiratory system (turbinate bones) to high elevation. Brain structure differed, particularly in the petrosal lobules of the cerebellum and the olfactory bulbs, between Otomyini and Gerbillinae, with extreme arid-adapted species in each clade being highly divergent (not convergent) from other species in the same clade. We observed greater "packing" of the maxillary turbinate bones, which have important respiratory functions, in Peromyscus mice from high and low elevations compared to the high-elevation African Praomyini, but more complex patterns within Peromyscus, probably related to trade-offs in respiratory physiology and heat exchange in the nasal epithelium associated with high-elevation adaptation.

Counter-gradient variation and the expensive tissue hypothesis explain parallel brain size reductions at high elevation in cricetid and murid rodents.

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.

Life history and habitat do not mediate temporal changes in body size due to climate warming in rodents.

Temporal changes in body size have been documented in a number of vertebrate species, with different contested drivers being suggested to explain these changes. Among these are climate warming, resource availability, competition, predation risk, human population density, island effects and others. Both life history traits (intrinsic factors such as lifespan and reproductive rate) and habitat (extrinsic factors such as vegetation type, latitude and elevation) are expected to mediate the existence of a significant temporal response of body size to climate warming but neither have been widely investigated. Using examples of rodents, we predicted that both life history traits and habitat might explain the probability of temporal response using two tests of this hypothesis. Firstly, taking advantage of new data from museum collections spanning the last 106 years, we investigated geographical and temporal variation in cranial size (a proxy for body size) in six African rodent species of two murid subfamilies (Murinae and Gerbillinae) of varying life history, degree of commensality, range size, and habitat. Two species, the commensal Mastomys natalensis, and the non-commensal Otomys unisulcatus showed significant temporal changes in body size, with the former increasing and the latter decreasing, in relation with climate warming. Commensalism could explain the increase in size with time due to steadily increasing food availability through increased agricultural production. Apart from this, we found no general life history or habitat predictors of a temporal response in African rodents. Secondly, in order to further test this hypothesis, we incorporated our data into a meta-analysis based on published literature on temporal responses in rodents, resulting in a combined dataset for 50 species from seven families worldwide; among these, 29 species showed no significant change, eight showed a significant increase in size, and 13 showed a decline in size. Using a binomial logistic regression model for these metadata, we found that none of our chosen life history or habitat predictors could significantly explain the probability of a temporal response to climate warming, reinforcing our conclusion based on the more detailed data from the six African species.

Associated tympanic bullar and cochlear hypertrophy define adaptations to true deserts in African gerbils and laminate-toothed rats (Muridae: Gerbillinae and Murinae).

Hearing capabilities in desert rodents such as gerbils and heteromyids have been inferred from both anatomical and ecological aspects and tested with experiments and theoretical models. However, very few studies have focused on other desert-adapted species. In this study, a refined three-dimensional morphometric approach was used on three African rodent tribes (Otomyini, Taterillini and Gerbillini) to describe the cochlear and tympanic bullar morphology, and to explore the role of phylogeny, allometry and ecology to better understand the underlying mechanism of any observed trends of hypertrophy in the bulla and associated changes in the cochlea. As a result, desert-adapted species could be distinguished from mesic and semi-arid taxa by the gross cochlear dimensions, particularly the oval window, which is larger in desert species. Bullar and cochlear modifications between species could be explained by environment (bulla and oval window), phylogeny (cochlear curvature gradient) and/or allometry (cochlear relative length, oval window and bulla) with some exceptions. Based on their ear anatomy, we predict that Desmodillus auricularis and Parotomys brantsii should be sensitive to low-frequency sounds, with D. auricularis sensitive to high-frequency sounds, too. This study concludes that in both arid and semi-arid adapted laminate-toothed rats and gerbils there is bulla and associated cochlea hypertrophy, particularly in true desert species. Gerbils also show tightly coiled cochlea but the significance of this is debatable and may have nothing to do with adaptations to any specific acoustics in the desert environment.