The decoupled nature of basal metabolic rate and body temperature in endotherm evolution

Avaria‐Llautureo, Jorge; Hernández, Cristián E.; Rodríguez‐Serrano, Enrique; Venditti, Chris

doi:10.1038/s41586-019-1476-9

Cited by 32 publications

(85 citation statements)

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“…Other studies provide relative data such as preserved apatite oxygen isotopes 24 that allow comparisons with co-habiting ectothermic taxa but cannot be directly compared to extant data and so do not suggest where the studied fossil taxa fall in the metabolic spectrum of extant vertebrates. However, our results are compatible with recent work on living mammals, suggesting that the BMR of the Middle Jurassic (∼170 Ma) mammalian MRCA was comparable to present-day values 13 . This indicates that evolution towards modern-day mammalian endothermy occurred during the 25 million year-long Early Jurassic and suggests that the mammalian mid-Jurassic adaptive radiation 4 , 5 was driven by this or vice versa.…”

Section: Discussionsupporting

confidence: 92%

“…Direct evidence from living mammals to support these hypotheses is equivocal 7 . Recent analyses find no long-term evolutionary trend in BMR 13 contradicting earlier suggestions of increasing BMR throughout the Cenozoic 12 and so implying that the Middle Jurassic (∼170 Ma) most recent common ancestor (MRCA) of living mammals 13 possessed a BMR within the range of present-day mammals. Several indirect indicators of metabolic physiology in fossil synapsids have been suggested but provide contradictory evidence for the timing of the origin of endothermy and its evolutionary tempo.…”

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confidence: 60%

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Reptile-like physiology in Early Jurassic stem-mammals

et al. 2020

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Despite considerable advances in knowledge of the anatomy, ecology and evolution of early mammals, far less is known about their physiology. Evidence is contradictory concerning the timing and fossil groups in which mammalian endothermy arose. To determine the state of metabolic evolution in two of the earliest stem-mammals, the Early Jurassic Morganucodon and Kuehneotherium, we use separate proxies for basal and maximum metabolic rate. Here we report, using synchrotron X-ray tomographic imaging of incremental tooth cementum, that they had maximum lifespans considerably longer than comparably sized living mammals, but similar to those of reptiles, and so they likely had reptilian-level basal metabolic rates. Measurements of femoral nutrient foramina show Morganucodon had blood flow rates intermediate between living mammals and reptiles, suggesting maximum metabolic rates increased evolutionarily before basal metabolic rates. Stem mammals lacked the elevated endothermic metabolism of living mammals, highlighting the mosaic nature of mammalian physiological evolution.

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Section: Discussionsupporting

confidence: 92%

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confidence: 60%

Reptile-like physiology in Early Jurassic stem-mammals

et al. 2020

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“…Other studies with relative data such as preserved apatite oxygen isotopes (22) allow comparisons with co-habiting ectothermic taxa but cannot be directly compared to extant data and cannot indicate where fossil taxa fall in the metabolic spectrum of extant vertebrates. However, our results are compatible with recent work on living mammals that the BMR of the Middle Jurassic (~170 Ma) mammalian MRCA was comparable to present-day values (14). This indicates evolution towards 5 modern-day mammalian endothermy occurred during the 25 million year-long Early Jurassic and suggests the mammalian mid-Jurassic adaptive radiation (5,6) was driven by this, or vice versa.…”

Section: Comparison Of Our Results To Other Recent Studies Of Physiolsupporting

confidence: 90%

Reptile-like physiology in Early Jurassic stem-mammals

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et al. 2019

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There is uncertainty regarding the timing and fossil species in which mammalian 5 endothermy arose, with few studies of stem-mammals on key aspects of endothermy such as basal or maximum metabolic rates, or placing them in the context of living vertebrate metabolic ranges. Synchrotron X-ray imaging of incremental tooth cementum shows two Early Jurassic stem-mammals, Morganucodon and Kuehneotherium, had lifespans (a basal metabolic rate proxy) considerably longer than comparably sized living mammals, but similar to reptiles, and 10 that Morganucodon had femoral blood flow rates (a maximum metabolic rate proxy) intermediate between living mammals and reptiles. This shows maximum metabolic rates increased evolutionarily before basal rates, and that contrary to previous suggestions of a Triassic origin, Early Jurassic stem-mammals lacked the endothermic metabolism of living mammals. 15 One Sentence Summary: Surprisingly long lifespans and low femoral blood flow suggest reptile-like physiology in key Early Jurassic stem-mammals. Main Text: Recent discoveries and analyses have revolutionized our knowledge of Mesozoic mammals, revealing novel aspects of their ecology (1, 2) development (3, 4) systematics (2, 4) 20and macroevolution (5,6). However, details of physiology are more difficult to determine from fossils, and our knowledge of physiological evolution remains comparatively poor. Living mammals are endotherms, possessing the ability to control and maintain metabolically produced 3 heat, and have a substantially higher capacity for sustained aerobic activity than ectothermic animals (7-9). The origin of endothermy is an important event in mammalian evolution, often noted as key to their success (7-9). Several competing hypotheses seek to explain the selective pressures and adaptive pathways of endothermic evolution: (a) selection for higher maximum metabolic rates (MMR) enhanced sustained aerobic activity (7, 10, 11); (b) selection for higher 5 basal metabolic rates (BMR) enhanced thermoregulatory control (12, 13); or (c) MMR and BMR evolved in lockstep with each other (8,9).Direct evidence from living mammals to support these hypotheses is equivocal (7).Recent analyses find no long-term evolutionary trend in BMR (14) contradicting earlier suggestions of increasing BMR throughout the Cenozoic (13), and so implying that the Middle 10 Jurassic (~170 Ma) most recent common ancestor (MRCA) of living mammals (14) possessed a BMR within the range of present-day mammals. Several indirect indicators of metabolic physiology in fossil synapsids have been suggested but provide contradictory evidence for the timing of origin of endothermy and its evolutionary tempo. These include: the presence of fibrolamellar long-bone, first seen in the Early Permian (~300 Ma) synapsid Ophiacodon (15); 15the presence of an infraorbital canal and lack of parietal foramen, used to infer facial whiskers, fur, lactation and endothermy in Early Triassic (~245 Ma) cynodonts (16); inferred maxillary nasal turbinates in the Late Permian (~255 Ma) th...

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“…The wide variation we found in r values within families also could be explained if we consider that the rates of evolution of body mass and echolocation call peak frequency in each family are decoupled, and these traits have followed different evolutionary pathways. In mammals, some features that should be coupled are not (Avaria‐Llautureo et al 2019), because each trait has different rates of evolution within clades (e.g. body mass; Arevalo et al 2020).…”

Section: Discussionmentioning

confidence: 99%

Does body mass restrict call peak frequency in echolocating bats?

et al. 2020

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1. Echolocation is the ability of some animals to orient themselves through sound emission and interpretation of the echoes. This is bats' main sense for orientation and recognising biotopes that provide food, water, and roosts. It is widely accepted that echolocation call frequency is related to body mass, and this relationship has been described as the 'allometric hypothesis', which proposes a negative correlation between these variables. 2. There is evidence that, in many cases, the allometric hypothesis does not apply. Additionally, studies supporting this hypothesis were done at the family level, resulting in a broad range of correlation values with r ranging from −0.36 to −0.76, and only insectivorous bats were included. Due to the notable exceptions and the lack of a quantitative synthesis of this hypothesis including all echolocating bats, we evaluated the allometric hypothesis of echolocation calls for this group. 3. Using a meta-analysis and phylogenetic generalised least-squares techniques, we evaluated the relationship between echolocation call peak frequency and the body mass of bats. 4. We found a negative relationship between body mass and echolocation call peak frequency for the 85 bat species that were included in our analysis (r = −0.3, p = 0.005). The relationship was consistent when we analysed the data at the insectivorous guild level, and in bats belonging to the families Vespertilionidae, Rhinolophidae, Emballonuridae, and the genus Myotis. However, the wide range of r values suggests that the strength of the relationship between peak frequency and body mass varies within the order Chiroptera. 5. Our results support the allometric hypothesis of sound production in echolocating bats. However, the low coefficient we found suggests that factors other than body mass may influence the peak frequency of echolocation calls produced by bats.

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The decoupled nature of basal metabolic rate and body temperature in endotherm evolution

Cited by 32 publications

References 28 publications

Reptile-like physiology in Early Jurassic stem-mammals

Reptile-like physiology in Early Jurassic stem-mammals

Reptile-like physiology in Early Jurassic stem-mammals

Does body mass restrict call peak frequency in echolocating bats?

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