1. Evolutionary Biology
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Coupling adaptive molecular evolution to phylodynamics using fitness-dependent birth-death models

  1. David A Rasmussen  Is a corresponding author
  2. Tanja Stadler
  1. North Carolina State University, United States
  2. ETH Zurich, Switzerland
Research Article
  • Cited 7
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Cite this article as: eLife 2019;8:e45562 doi: 10.7554/eLife.45562

Abstract

Beneficial and deleterious mutations cause the fitness of lineages to vary across a phylogeny and thereby shape its branching structure. While standard phylogenetic models do not allow mutations to feedback and shape trees, birth-death models can account for this feedback by letting the fitness of lineages depend on their type. To date, these multi-type birth-death models have only been applied to cases where a lineage's fitness is determined by a single character state. We extend these models to track sequence evolution at multiple sites. This approach remains computationally tractable by tracking the genotype and fitness of lineages probabilistically in an approximate manner. Although approximate, we show that we can accurately estimate the fitness of lineages and site-specific mutational fitness effects from phylogenies. We apply this approach to estimate the population-level fitness effects of mutations in Ebola and influenza virus, and compare our estimates with in vitro fitness measurements for these mutations.

Data availability

All data and code required to reproduce our Ebola analysis in its entirety is available at https://github.com/davidrasm/Lumiere/tree/master/ebola. The sequence alignment along with the timecalibrated molecular phylogeny we used for our analysis were downloaded from https://github.com/ebov/space-time/tree/master/Data. Dataset S3 of Lee et al. 2018 was downloaded from https://www.pnas.org/highwire/filestream/822898/field_highwire_adjunct_files/3/pnas.1806133115.sd03.xlsx.

Article and author information

Author details

  1. David A Rasmussen

    Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, 27607, United States
    For correspondence
    drasmus@ncsu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9457-7561
  2. Tanja Stadler

    Department of Biosystems Science and Engineering, ETH Zurich, Basel, Switzerland
    Competing interests
    The authors declare that no competing interests exist.

Funding

Seventh Framework Programme (European Research Commission)

  • Tanja Stadler

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Aleksandra M Walczak, École Normale Supérieure, France

Publication history

  1. Received: January 27, 2019
  2. Accepted: July 26, 2019
  3. Accepted Manuscript published: August 14, 2019 (version 1)
  4. Accepted Manuscript updated: August 15, 2019 (version 2)
  5. Version of Record published: August 29, 2019 (version 3)

Copyright

© 2019, Rasmussen & Stadler

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

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Further reading

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    Dinosaur bonebeds with amber content, yet scarce, offer a superior wealth and quality of data on ancient terrestrial ecosystems. However, the preserved palaeodiversity and/or taphonomic characteristics of these exceptional localities had hitherto limited their palaeobiological potential. Here, we describe the amber from the Lower Cretaceous dinosaur bonebed of Ariño (Teruel, Spain) using a multidisciplinary approach. Amber is found in both a root layer with amber strictly in situ and a litter layer mainly composed of aerial pieces unusually rich in bioinclusions, encompassing 11 insect orders, arachnids, and a few plant and vertebrate remains, including a feather. Additional palaeontological data—charophytes, palynomorphs, ostracods— are provided. Ariño arguably represents the most prolific and palaeobiologically diverse locality in which fossiliferous amber and a dinosaur bonebed have been found in association, and the only one known where the vast majority of the palaeontological assemblage suffered no or low-grade pre-burial transport. This has unlocked unprecedentedly complete and reliable palaeoecological data out of two complementary windows of preservation—the bonebed and the amber—from the same site.

    1. Evolutionary Biology
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    The mechanics of Dipteran thorax is dictated by a network of exoskeletal linkages that, when deformed by the flight muscles, generate coordinated wing movements. In Diptera, the forewings power flight, whereas the hindwings have evolved into specialized structures called halteres, which provide rapid mechanosensory feedback for flight stabilization. Although actuated by independent muscles, wing and haltere motion is precisely phase-coordinated at high frequencies. Because wingbeat frequency is a product of wing-thorax resonance, any wear-and-tear of wings or thorax should impair flight ability. How robust is the Dipteran flight system against such perturbations? Here, we show that wings and halteres are independently driven, coupled oscillators. We systematically reduced the wing length in flies and observed how wing-haltere synchronization was affected. The wing-wing system is a strongly coupled oscillator, whereas the wing-haltere system is weakly coupled through mechanical linkages that synchronize phase and frequency. Wing-haltere link acts in a unidirectional manner; altering wingbeat frequency affects haltere frequency, but not vice versa. Exoskeletal linkages are thus key morphological features of the Dipteran thorax that ensure wing-haltere synchrony, despite severe wing damage.