Evolution: Mapping the ancestry of primates

Structures in the inner ear can help determine the evolutionary relationship between extinct and living primates.
  1. Ignacio Martínez  Is a corresponding author
  2. Mercedes Conde-Valverde
  1. Cátedra de Otoacústica Evolutiva y Paleoantropología, HM Hospitales - Universidad de Alcalá, Spain

When the term ‘primates’ was originally coined by Carl Linneus back in 1758, it was to classify all species of monkeys, humans and apes into one group based on their anatomical similarities. At that time, the observed similarities were simply a curiosity and did not imply any special relationship between these species. Later, when Charles Darwin published ‘On the Origin of Species’ in 1859, it became clear that species with comparable anatomies are often evolutionarily linked. And when Thomas Huxley published 'Evidence as to Man’s Place in Nature' in 1863, he grouped humans, gibbons, orangutans, gorillas and chimpanzees into a superfamily named the Hominoidea. Since then, understanding the evolutionary relationships within this superfamily has been a fundamental part of research on human evolution.

Extant members of this family, also known as hominoids, can be arranged into two families: the Hylobatidae family, which includes gibbons; and the Hominidae family, which includes orangutans, gorillas, chimpanzees and humans (Figure 1). About 16 to 7 million years ago, during the middle and upper Miocene period, hominoids expanded throughout Europe, Africa and Asia, and diversified into at least 12 different species which have now become extinct (Begun et al., 2012). Fossils from this time led to the identification of a particularly intriguing species called Oreopithecus bambolii (Moyà-Solà et al., 2004; Moyà-Solà et al., 2009).

The evolutionary relationship between O. bambolii and the Hominidae family.

Non-extinct members of the Hominoidea superfamily are split into two families: the Hominidae family, which includes orangutans (Pongo), gorillas (Gorilla), chimpanzees (Pan) and humans (Homo); and the Hylobatidae family, which includes various gibbons (Hylotbates, Nomascus, Symphalangus and Hoolok). However, it is not clear if the extinct species Oreopithecus bambolii split from this branch of the tree of life after the Hylobatidae family split, in which case O. bambolii could be part of Hominidae family (A), or if it split before the Hylobatidae family split (B). Uriciuoli et al. found that O. bambolii is not part of the Hominidae family (that is, scenario B).

O. bambolii fossils date back about 8 million years and come from sites in Sardinia and Tuscany (Rook et al., 2011). The varied features within these fossils have made it difficult to determine the evolutionary history of O. bambolii and its relationship to living hominoid species (Harrison and Rook, 1997; Köhler and Moyà-Solà, 1997). As a result, there is an ongoing debate about whether or not O. bambolii should be included in the Hominidae family (Begun et al., 2012; Nengo et al., 2017). The key to solving this question is to establish how closely related O. bambolii are to the Hominidae family compared to gibbons (Figure 1).

Now, in eLife, David Alba (Institut Català de Paleontologia Miquel Crusafont of the Universitat Autònoma de Barcelona) and colleagues – including Alessandro Urciuoli (Barcelona) as first author, and researchers in France and South Africa – report how studying the shape of semicircular canals in the ears of non-extinct primates can provide a better understanding of how the hominoid family evolved over time (Urciuoli et al., 2020). In recent years, these canals (which form part of the bony exterior of the inner ear) have been used to determine the degree of similarity between members of the Hominidae family (Ponce de León et al., 2018; Quam et al., 2016; Beaudet et al., 2019).

The team reconstructed the three-dimensional shape of semicircular canals of 27 species of living primates and two extinct species, including the O. bambolii. This revealed that structures in the inner ear can be used to study the evolutionary relationships between living and extinct hominoid species.

Urciuoli et al. found that although the semicircular canals of O. bambolii had similar characteristics to hominoids, this anatomical region had more features in common with two other primate families known as the cercopithecoids and platyrrhines. This suggests that O. bambolii are evolutionarily further away from orangutans, gorillas, chimpanzees and humans than gibbons, and therefore cannot be considered a true member of the Hominidae family (Figure 1B).

The next step will be to study the semicircular canals of other extinct hominoid species, and repeat the experiment using other anatomical regions in the inner ear, such as the cochlea.

References

    1. Harrison T
    2. Rook L
    (1997)
    Function, Phylogeny, and Fossils. Advances in Primatology
    Enigmatic anthropoid or misunderstood ape? The phylogenetic status of Oreopithecus bambolii reconsidered, Function, Phylogeny, and Fossils. Advances in Primatology, Boston, MA, Springer, 10.1007/978-1-4899-0075-3.

Article and author information

Author details

  1. Ignacio Martínez

    Ignacio Martínez is in the Cátedra de Otoacústica Evolutiva y Paleoantropología, HM Hospitales - Universidad de Alcalá, Madrid, Spain

    For correspondence
    ignacio.martinezm@uah.es
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1835-9199
  2. Mercedes Conde-Valverde

    Mercedes Conde-Valverde is in the Cátedra de Otoacústica Evolutiva y Paleoantropología, HM Hospitales - Universidad de Alcalá, Madrid, Spain

    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1891-5324

Publication history

  1. Version of Record published:

Copyright

© 2020, Martínez and Conde-Valverde

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 6,331
    views
  • 186
    downloads
  • 0
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Ignacio Martínez
  2. Mercedes Conde-Valverde
(2020)
Evolution: Mapping the ancestry of primates
eLife 9:e55429.
https://doi.org/10.7554/eLife.55429
  1. Further reading

Further reading

    1. Computational and Systems Biology
    2. Evolutionary Biology
    Kara Schmidlin, Sam Apodaca ... Kerry Geiler-Samerotte
    Research Article

    There is growing interest in designing multidrug therapies that leverage tradeoffs to combat resistance. Tradeoffs are common in evolution and occur when, for example, resistance to one drug results in sensitivity to another. Major questions remain about the extent to which tradeoffs are reliable, specifically, whether the mutants that provide resistance to a given drug all suffer similar tradeoffs. This question is difficult because the drug-resistant mutants observed in the clinic, and even those evolved in controlled laboratory settings, are often biased towards those that provide large fitness benefits. Thus, the mutations (and mechanisms) that provide drug resistance may be more diverse than current data suggests. Here, we perform evolution experiments utilizing lineage-tracking to capture a fuller spectrum of mutations that give yeast cells a fitness advantage in fluconazole, a common antifungal drug. We then quantify fitness tradeoffs for each of 774 evolved mutants across 12 environments, finding these mutants group into classes with characteristically different tradeoffs. Their unique tradeoffs may imply that each group of mutants affects fitness through different underlying mechanisms. Some of the groupings we find are surprising. For example, we find some mutants that resist single drugs do not resist their combination, while others do. And some mutants to the same gene have different tradeoffs than others. These findings, on one hand, demonstrate the difficulty in relying on consistent or intuitive tradeoffs when designing multidrug treatments. On the other hand, by demonstrating that hundreds of adaptive mutations can be reduced to a few groups with characteristic tradeoffs, our findings may yet empower multidrug strategies that leverage tradeoffs to combat resistance. More generally speaking, by grouping mutants that likely affect fitness through similar underlying mechanisms, our work guides efforts to map the phenotypic effects of mutation.

    1. Evolutionary Biology
    2. Microbiology and Infectious Disease
    Zachary H Williams, Alvaro Dafonte Imedio ... Welkin E Johnson
    Research Article Updated

    HERV-K(HML-2), the youngest clade of human endogenous retroviruses (HERVs), includes many intact or nearly intact proviruses, but no replication competent HML-2 proviruses have been identified in humans. HML-2-related proviruses are present in other primates, including rhesus macaques, but the extent and timing of HML-2 activity in macaques remains unclear. We have identified 145 HML-2-like proviruses in rhesus macaques, including a clade of young, rhesus-specific insertions. Age estimates, intact open reading frames, and insertional polymorphism of these insertions are consistent with recent or ongoing infectious activity in macaques. 106 of the proviruses form a clade characterized by an ~750 bp sequence between env and the 3′ long terminal repeat (LTR), derived from an ancient recombination with a HERV-K(HML-8)-related virus. This clade is found in Old World monkeys (OWM), but not great apes, suggesting it originated after the ape/OWM split. We identified similar proviruses in white-cheeked gibbons; the gibbon insertions cluster within the OWM recombinant clade, suggesting interspecies transmission from OWM to gibbons. The LTRs of the youngest proviruses have deletions in U3, which disrupt the Rec Response Element (RcRE), required for nuclear export of unspliced viral RNA. We show that the HML-8-derived region functions as a Rec-independent constitutive transport element (CTE), indicating the ancestral Rec–RcRE export system was replaced by a CTE mechanism.