Molecular dating of the blood pigment hemocyanin provides new insight into the origin of animals

Costa-Paiva, Elisa Maria; Mello, Beatriz; Bezerra, Bruno Santos; Coates, Christopher J.; Halanych, Kenneth M.; Brown, Federico D.; Leme, Juliana de Moraes; Trindade, R. I.

doi:10.1111/gbi.12481

Cited by 6 publications

(5 citation statements)

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“…Divergence time estimates are applied to gene trees to infer the origin of various physiological modalities. Consequently, our understanding of the tempo and mode of early animal evolution can be enhanced by molecular dating of specific genes and proteins (Shih & Matzke, 2013; Yu & Li, 2014; Bezerra et al, 2021; Boden et al, 2021; Costa‐Paiva et al, 2021).…”

Section: Introductionmentioning

confidence: 99%

Divergence time estimates for the hypoxia‐inducible factor‐1 alpha (HIF1α) reveal an ancient emergence of animals in low‐oxygen environments

Belato,

Mello,

Coates

et al. 2023

Geobiology

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Unveiling the tempo and mode of animal evolution is necessary to understand the links between environmental changes and biological innovation. Although the earliest unambiguous metazoan fossils date to the late Ediacaran period, molecular clock estimates agree that the last common ancestor (LCA) of all extant animals emerged ~850 Ma, in the Tonian period, before the oldest evidence for widespread ocean oxygenation at ~635–560 Ma in the Ediacaran period. Metazoans are aerobic organisms, that is, they are dependent on oxygen to survive. In low‐oxygen conditions, most animals have an evolutionarily conserved pathway for maintaining oxygen homeostasis that triggers physiological changes in gene expression via the hypoxia‐inducible factor (HIFa). However, here we confirm the absence of the characteristic HIFa protein domain responsible for the oxygen sensing of HIFa in sponges and ctenophores, indicating the LCA of metazoans lacked the functional protein domain as well, and so could have maintained their transcription levels unaltered under the very low‐oxygen concentrations of their environments. Using Bayesian relaxed molecular clock dating, we inferred that the ancestral gene lineage responsible for HIFa arose in the Mesoproterozoic Era, ~1273 Ma (Credibility Interval 957–1621 Ma), consistent with the idea that important genetic machinery associated with animals evolved much earlier than the LCA of animals. Our data suggest at least two duplication events in the evolutionary history of HIFa, which generated three vertebrate paralogs, products of the two successive whole‐genome duplications that occurred in the vertebrate LCA. Overall, our results support the hypothesis of a pre‐Tonian emergence of metazoans under low‐oxygen conditions, and an increase in oxygen response elements during animal evolution.

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Section: Introductionmentioning

confidence: 99%

Divergence time estimates for the hypoxia‐inducible factor‐1 alpha (HIF1α) reveal an ancient emergence of animals in low‐oxygen environments

Belato,

Mello,

Coates

et al. 2023

Geobiology

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“…Stem‐group eumetazoans are first found widespread in the fossil record around 572–602 Ma (Budd & Jensen, 2017 ; Dunn et al, 2021 ; Wood et al, 2019 ; Yang et al, 2022 ), yet recent molecular clock studies suggest a much earlier metazoan origination time of around 800–850 Ma (Beavan et al, 2021 ; Dohrmann & Wörheide, 2017 ; dos Reis et al, 2015 ; Maria Costa‐Paiva et al, 2022 ; Figure 1 ). Given the inherent patchiness of the fossil record and the uncertainties of molecular clock estimates (Budd & Mann, 2020 ; dos Reis et al, 2015 ) the exact timing of this key evolutionary milestone is hard to resolve.…”

Section: Introductionmentioning

confidence: 99%

“…Given the inherent patchiness of the fossil record and the uncertainties of molecular clock estimates (Budd & Mann, 2020 ; dos Reis et al, 2015 ) the exact timing of this key evolutionary milestone is hard to resolve. The recent discovery of a putative fossil keratose sponge (~890 Ma) (Turner, 2021 ) and the molecular dating of the blood pigment hemocyanin to 881 Ma would push back the inception of animals by around 200 million years (Maria Costa‐Paiva et al, 2022 ). Even the most conservative molecular clock estimates push the origins of animal life to the edge of the Ediacaran Gaskiers glaciation (a so‐called slushball Earth ~580 Ma), whereas estimates beyond 720 Ma would require life to have this survived two further global glaciation events (Marinoan and Sturtian snowball Earths) during the Cryogenian (Peterson et al, 2004 ).…”

Section: Introductionmentioning

confidence: 99%

Animal survival strategies in Neoproterozoic ice worlds

Griffiths

Whittle

Mitchell

2022

Global Change Biology

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The timing of the first appearance of animals is of crucial importance for understanding the evolution of life on Earth. Although the fossil record places the earliest metazoans at 572-602 Ma, molecular clock studies suggest a far earlier origination, as far back as ~850 Ma. The difference in these dates would place the rise of animal life into a time period punctuated by multiple colossal, potentially global, glacial events.Although the two schools of thought debate the limitations of each other's methods, little time has been dedicated to how animal life might have survived if it did arise before or during these global glacial periods. The history of recent polar biota shows that organisms have found ways of persisting on and around the ice of the Antarctic continent throughout the Last Glacial Maximum (33-14 Ka), with some endemic species present before the breakup of Gondwana (180-23 Ma). Here we discuss the survival strategies and habitats of modern polar marine organisms in environments analogous to those that could have existed during Neoproterozoic glaciations. We discuss how, despite the apparent harshness of many ice covered, sub-zero, Antarctic marine habitats, animal life thrives on, in and under the ice. Ice dominated systems and processes make some local environments more habitable through water circulation, oxygenation, terrigenous nutrient input and novel habitats. We consider how the physical conditions of Neoproterozoic glaciations would likely have dramatically impacted conditions for potential life in the shallows and erased any possible fossil evidence from the continental shelves. The recent glacial cycle has driven the evolution of Antarctica's unique fauna by acting as a "diversity pump," and the same could be true for the late Proterozoic and the evolution of animal life on Earth, and the existence of life elsewhere in the universe on icy worlds or moons.

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“…This framework of the early metazoan evolution inferred from the combined data of genetics and development, together with that from paleontology itself, has profoundly influenced the paleontologic community. For example, it has been accelerating the shift of the community focus from the early Cambrian animals to the records of Ediacaran, Cryogenian, or even Tonian (Knoll and Carroll, 1999;Mills et al, 2018), the periods during which metazoans are predicted to have originated and diverged (Yang et al, 2007;Peterson et al, 2008;Reis et al, 2015;Lozano-Fernandez et al, 2017;Costa-Paiva et al, 2022). Searching for representatives of extant phyla in the Neoproterozoic strata is becoming more promising, as exemplified by recent discoveries of bilaterian fossils (Chen et al, 2019;Evans et al, 2020) and crown cnidarian in Ediacaran (Dunn et al, 2022).…”

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confidence: 99%

The early animal radiation: insights from interpreting the Cambrian problematic fossils

Peng

2023

Front. Earth Sci.

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Genic and genomic data have been reshaping our understanding of the earliest radiation event of metazoans, the well-known Cambrian Evolutionary Radiation, not only from the respects of reshuffling the phylogenetic topologies of some animal phyla but by deciphering the deep homologies of many morphological features. These advances, together with the continuing discoveries of the Ediacaran-Cambrian fossils, are unveiling the cladogenetic process of the early metazoans and the patterns of morphologic evolution during this biological radiation event. In this review, I focus on a small but challenging field, the problematic fossils from the early Cambrian fossil Lagerstätten, such as the Chengjiang biota, mainly on the controversies concerning their interpretation and the consequent impacts on understanding the early evolution of animals. The bizarre body plans of the early Cambrian problematica alone do not account for the difficulties in studying their biology and affinity. Instead, it is the combined action of the taphonomic artifacts and the uncertainty in homologizing the preserved characters that impede generating plausible interpretations. Despite all these issues, a testable and repeatable method for interpreting fossils has emerged and is becoming more practicable. The integration of an evolutionary-grade conceptual frame is beneficial to the interpretation of the Cambrian problematic fossils. Together with the focus on taphonomic alternation and homologic assessment, the Cambrian problematic fossils are becoming more informative nodes in the “parsing tree” of early animal evolution.

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Molecular dating of the blood pigment hemocyanin provides new insight into the origin of animals

Cited by 6 publications

References 127 publications

Divergence time estimates for the hypoxia‐inducible factor‐1 alpha (HIF1α) reveal an ancient emergence of animals in low‐oxygen environments

Divergence time estimates for the hypoxia‐inducible factor‐1 alpha (HIF1α) reveal an ancient emergence of animals in low‐oxygen environments

Animal survival strategies in Neoproterozoic ice worlds

The early animal radiation: insights from interpreting the Cambrian problematic fossils

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