TY - JOUR

T1 - Convergent evolution of increased urine-concentrating ability in desert mammals

AU - Rocha, Joana L.

AU - Brito, José C.

AU - Nielsen, Rasmus

AU - Godinho, Raquel

N1 - Funding Information: We thank Pedro Tarroso and Antigoni Kaliontzopoulou for discussions that helped us conceive this study. J.L.R., J.C.B and R.G. were supported by the Portuguese Foundation for Science and Technology (SFRH/BD/116397/2016, CEECINST/00014/2018, and DL57/2016, respectively). This work was partially supported by FCT project PTDC/BIA‐EVL/31902/2017. Publisher Copyright: © 2021 The Authors. Mammal Review published by Mammal Society and John Wiley & Sons Ltd.

PY - 2021

Y1 - 2021

N2 - One of the most celebrated textbook examples of physiological adaptations to desert environments is the unique ability that desert mammals have to produce hyperosmotic urine. Commonly perceived as an adaptation mainly observed in small rodents, the extent to which urine-concentrating ability has evolved independently in distinct mammalian lineages has not previously been assessed using modern phylogenetic approaches. We review urine-concentrating ability data from the literature in 121 mammalian species with geographic ranges encompassing varying climatic conditions. We explicitly test the general hypothesis that desert-dwelling mammals have evolved greater ability to concentrate urine than non-desert species, controlling for body mass, phylogenetic affinity and other covariates. Ancestral state reconstruction across our dataset’s phylogeny shows that the ability to produce hyperosmotic urine, measured as maximum urine osmolality, has evolved convergently in mammalian species with geographic ranges characterised by low mean annual aridity index. Phylogenetic generalised least-squares (PGLS) models show that the mean annual aridity index of a species’ geographic range largely predicts its urine-concentrating ability, even when accounting for body mass differences, phylogenetic correlations, the specific condition under which urine osmolality was measured, the method used to measure urine osmolality, and the species’ diet. In contrast, we find much weaker correlations between mass-adjusted basal metabolic rate and environmental variables when analysing 84 of the species included in the urine osmolality analysis. Taken together, our results not only show that desert mammals effectively concentrate more urine than non-desert mammals, but further suggest that aridity is likely to have been one of the main selective pressures leading to increasing maximum urine-concentrating ability and driving its repeated evolution in different desert mammalian lineages.

AB - One of the most celebrated textbook examples of physiological adaptations to desert environments is the unique ability that desert mammals have to produce hyperosmotic urine. Commonly perceived as an adaptation mainly observed in small rodents, the extent to which urine-concentrating ability has evolved independently in distinct mammalian lineages has not previously been assessed using modern phylogenetic approaches. We review urine-concentrating ability data from the literature in 121 mammalian species with geographic ranges encompassing varying climatic conditions. We explicitly test the general hypothesis that desert-dwelling mammals have evolved greater ability to concentrate urine than non-desert species, controlling for body mass, phylogenetic affinity and other covariates. Ancestral state reconstruction across our dataset’s phylogeny shows that the ability to produce hyperosmotic urine, measured as maximum urine osmolality, has evolved convergently in mammalian species with geographic ranges characterised by low mean annual aridity index. Phylogenetic generalised least-squares (PGLS) models show that the mean annual aridity index of a species’ geographic range largely predicts its urine-concentrating ability, even when accounting for body mass differences, phylogenetic correlations, the specific condition under which urine osmolality was measured, the method used to measure urine osmolality, and the species’ diet. In contrast, we find much weaker correlations between mass-adjusted basal metabolic rate and environmental variables when analysing 84 of the species included in the urine osmolality analysis. Taken together, our results not only show that desert mammals effectively concentrate more urine than non-desert mammals, but further suggest that aridity is likely to have been one of the main selective pressures leading to increasing maximum urine-concentrating ability and driving its repeated evolution in different desert mammalian lineages.

KW - adaptation

KW - aridity index

KW - convergent evolution

KW - deserts

KW - hyperosmotic urine

KW - mammals

KW - phylogenetic generalised least-squares (PGLS) models

U2 - 10.1111/mam.12244

DO - 10.1111/mam.12244

M3 - Review

AN - SCOPUS:85101806854

VL - 51

SP - 482

EP - 491

JO - Mammal Review

JF - Mammal Review

SN - 0305-1838

IS - 4

ER -