Convergent evolution of increased urine‐concentrating ability in desert mammals

Abstract

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.

Life in Deserts: The Genetic Basis of Mammalian Desert Adaptation

“…Some genes from this pathway putatively under selection (Figure 1D) may be involved in the production of vasodilators of renal preglomerular vessels [19(S)-HETE] that simulate water reabsorption at the kidney. These results hold exciting promise for further investigation of genetic changes underlying the outstanding urine-concentrating ability of desert mammals [7].…”

“…Mammalian evaders include small rodents that can avoid overheating by being nocturnal and hiding in burrows during the day, and are less reliant on evaporative cooling [2]. Evaders can additionally minimize water loss by concentrating highly hyperosmotic urine with low volume [7] and utilize water derived from fat metabolism (metabolic water) well beyond the abilities of non-desert counterparts (Table I for examples) [2,65].…”

“…Evaporator species have enlarged body extremities (e.g., large ears) to dissipate heat by conduction and use denning and nocturnal behavior to avoid extreme heat. They also have significantly low mass-adjusted nonrenal water loss [1,2] and can minimize renal water loss by concentrating highly hyperosmotic urine significantly above the levels seen in nondesert counterparts [2,7]. However, some authors have criticized this categorization due to overlap between the categories and have proposed other frameworks to synthesize desert mammalian phenotypic adaptations (e.g., [6]).…”

“…However, some authors have criticized this categorization due to overlap between the categories and have proposed other frameworks to synthesize desert mammalian phenotypic adaptations (e.g., [6]). Water Increased vasopressin En (1,8), Ev (1,6,10) ; Increased aldosterone En (1,3,4), Ev (3,4) Increased urine osmolality/Increased water reabsorption from the kidney En (1,2), Ev, Evap (1,4) ; decreased urine production Ev (1,5,7) Reduced aldosterone En (1) Increased urine sodium excretion En (1) Low glomerular filtration rate En (1,3), Ev (2,5,7) Higher levels of plasma creatinine with no apparent kidney damage or renal impairment En (1,2), Ev (5,7) Higher urea En (1,2), Ev (5,7) , glucose En (1,7), potassium Ev (7) , sodium En (1) , and chloride Ev (5,7) Increased plasma osmolality En (1,2), Ev (1, 5,7,10), Evap (5) Food/water Increased fat storage in body tissues En (1,7,7 ,4) Energy reservation during food/water scarcity Fat metabolism En (1,2,4,7), Ev (13,14) Enhanced use of metabolic water En (1,2,7), Ev (1,2,8, 12,13,14), Evap (1,2) Higher plasma sodium En (1) Tolerance of high-salt diet En (1,6,7 ), Ev (1,4,8,9), Evap (5) Decreased insulin secretion without diabetes Ev (1) Adaptive tolerance to dehydration and starvation [ 17,21,32,…”

“…The organismal responses required to survive these extreme conditions for multiple generations are usually outside the range of the plastic responses of most non-desert species. Thus, it is generally presumed that desert-adapted species likely experienced strong selection acting on various complex phenotypes related to metabolism and water retention [1,2,[6][7][8].…”