Dataset Information

Whole-body endothermy: ancient, homologous and widespread among the ancestors of mammals, birds and crocodylians.

ABSTRACT: The whole-body (tachymetabolic) endothermy seen in modern birds and mammals is long held to have evolved independently in each group, a reasonable assumption when it was believed that its earliest appearances in birds and mammals arose many millions of years apart. That assumption is consistent with current acceptance that the non-shivering thermogenesis (NST) component of regulatory body heat originates differently in each group: from skeletal muscle in birds and from brown adipose tissue (BAT) in mammals. However, BAT is absent in monotremes, marsupials, and many eutherians, all whole-body endotherms. Indeed, recent research implies that BAT-driven NST originated more recently and that the biochemical processes driving muscle NST in birds, many modern mammals and the ancestors of both may be similar, deriving from controlled 'slippage' of Ca²⁺ from the sarcoplasmic reticulum Ca²⁺ -ATPase (SERCA) in skeletal muscle, similar to a process seen in some fishes. This similarity prompted our realisation that the capacity for whole-body endothermy could even have pre-dated the divergence of Amniota into Synapsida and Sauropsida, leading us to hypothesise the homology of whole-body endothermy in birds and mammals, in contrast to the current assumption of their independent (convergent) evolution. To explore the extent of similarity between muscle NST in mammals and birds we undertook a detailed review of these processes and their control in each group. We found considerable but not complete similarity between them: in extant mammals the 'slippage' is controlled by the protein sarcolipin (SLN), in birds the SLN is slightly different structurally and its role in NST is not yet proved. However, considering the multi-millions of years since the separation of synapsids and diapsids, we consider that the similarity between NST production in birds and mammals is consistent with their whole-body endothermy being homologous. If so, we should expect to find evidence for it much earlier and more widespread among extinct amniotes than is currently recognised. Accordingly, we conducted an extensive survey of the palaeontological literature using established proxies. Fossil bone histology reveals evidence of sustained rapid growth rates indicating tachymetabolism. Large body size and erect stature indicate high systemic arterial blood pressures and four-chambered hearts, characteristic of tachymetabolism. Large nutrient foramina in long bones are indicative of high bone perfusion for rapid somatic growth and for repair of microfractures caused by intense locomotion. Obligate bipedality appeared early and only in whole-body endotherms. Isotopic profiles of fossil material indicate endothermic levels of body temperature. These proxies led us to compelling evidence for the widespread occurrence of whole-body endothermy among numerous extinct synapsids and sauropsids, and very early in each clade's family tree. These results are consistent with and support our hypothesis that tachymetabolic endothermy is plesiomorphic in Amniota. A hypothetical structure for the heart of the earliest endothermic amniotes is proposed. We conclude that there is strong evidence for whole-body endothermy being ancient and widespread among amniotes and that the similarity of biochemical processes driving muscle NST in extant birds and mammals strengthens the case for its plesiomorphy.

SUBMITTER: Grigg G

PROVIDER: S-EPMC9300183 | biostudies-literature |

REPOSITORIES: biostudies-literature

ACCESS DATA

Similar Datasets

Project description:1. The power-law dependence of metabolic rate on body mass has major implications at every level of ecological organization. However, the overwhelming majority of studies examining this relationship have used basal or resting metabolic rates, and/or have used data consisting of species-averaged masses and metabolic rates. Field metabolic rates are more ecologically relevant and are probably more directly subject to natural selection than basal rates. Individual rates might be more important than species-average rates in determining the outcome of ecological interactions, and hence selection. 2. We here provide the first comprehensive database of published field metabolic rates and body masses of individual birds and mammals, containing measurements of 1498 animals of 133 species in 28 orders. We used linear mixed-effects models to answer questions about the body mass scaling of metabolic rate and its taxonomic universality/heterogeneity that have become classic areas of controversy. Our statistical approach allows mean scaling exponents and taxonomic heterogeneity in scaling to be analysed in a unified way while simultaneously accounting for nonindependence in the data due to shared evolutionary history of related species. 3. The mean power-law scaling exponents of metabolic rate vs. body mass relationships were 0.71 [95% confidence intervals (CI) 0.625-0.795] for birds and 0.64 (95% CI 0.564-0.716) for mammals. However, these central tendencies obscured meaningful taxonomic heterogeneity in scaling exponents. The primary taxonomic level at which heterogeneity occurred was the order level. Substantial heterogeneity also occurred at the species level, a fact that cannot be revealed by species-averaged data sets used in prior work. Variability in scaling exponents at both order and species levels was comparable to or exceeded the differences 3/4-2/3 = 1/12 and 0.71-0.64. 4. Results are interpreted in the light of a variety of existing theories. In particular, results are consistent with the heat dissipation theory of Speakman & Król (2010) and provided some support for the metabolic levels boundary hypothesis of Glazier (2010). 5. Our analysis provides the first comprehensive empirical analysis of the scaling relationship between field metabolic rate and body mass in individual birds and mammals. Our data set is a valuable contribution to those interested in theories of the allometry of metabolic rates.

Project description:BackgroundThe genomic history of prokaryotic organismal lineages is marked by extensive horizontal gene transfer (HGT) between groups of organisms at all taxonomic levels. These HGT events have played an essential role in the origin and distribution of biological innovations. Analyses of ancient gene families show that HGT existed in the distant past, even at the time of the organismal last universal common ancestor (LUCA). Most gene transfers originated in lineages that have since gone extinct. Therefore, one cannot assume that the last common ancestors of each gene were all present in the same cell representing the cellular ancestor of all extant life.ResultsOrganisms existing as part of a diverse ecosystem at the time of LUCA likely shared genetic material between lineages. If these other lineages persisted for some time, HGT with the descendants of LUCA could have continued into the bacterial and archaeal lineages. Phylogenetic analyses of aminoacyl-tRNA synthetase protein families support the hypothesis that the molecular common ancestors of the most ancient gene families did not all coincide in space and time. This is most apparent in the evolutionary histories of seryl-tRNA synthetase and threonyl-tRNA synthetase protein families, each containing highly divergent "rare" forms, as well as the sparse phylogenetic distributions of pyrrolysyl-tRNA synthetase, and the bacterial heterodimeric form of glycyl-tRNA synthetase. These topologies and phyletic distributions are consistent with horizontal transfers from ancient, likely extinct branches of the tree of life.ConclusionsOf all the organisms that may have existed at the time of LUCA, by definition only one lineage is survived by known progeny; however, this lineage retains a genomic record of heterogeneous genetic origins. The evolutionary histories of aminoacyl-tRNA synthetases (aaRS) are especially informative in detecting this signal, as they perform primordial biological functions, have undergone several ancient HGT events, and contain many sites with low substitution rates allowing deep phylogenetic reconstruction. We conclude that some aaRS families contain groups that diverge before LUCA. We propose that these ancient gene variants be described by the term "hypnologs", reflecting their ancient, reticulate origin from a time in life history that has been all but erased".

Dataset Information

Whole-body endothermy: ancient, homologous and widespread among the ancestors of mammals, birds and crocodylians.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets