Multifactorial processes underlie parallel opsin loss in neotropical bats
- University of California, Los Angeles, United States
- Queen Mary University of London, United Kingdom
- Stony Brook University, United States
- University of Illinois, United States
- Harvard University, United States
- University of California, Merced, United States
Abstract
The loss of previously adaptive traits is typically linked to relaxation in selection, yet the molecular steps leading to such repeated losses are rarely known. Molecular studies of loss have tended to focus on gene sequences alone, but overlooking other aspects of protein expression might underestimate phenotypic diversity. Insights based almost solely on opsin gene evolution, for instance, have made mammalian color vision a textbook example of phenotypic loss. We address this gap by investigating retention and loss of opsin genes, transcripts and proteins across ecologically diverse noctilionoid bats. We find multiple, independent losses of short-wave sensitive opsins. Mismatches between putatively functional DNA sequences, mRNA transcripts, and proteins implicate transcriptional and post-transcriptional processes in the ongoing loss of S-opsins in some noctilionoid bats. Our results provide a snapshot of evolution in progress during phenotypic trait loss, and suggest vertebrate visual phenotypes cannot always be predicted from genotypes alone.
Data availability
Sequencing data have been deposited in GenBank in the Nucleotide Database. The accession numbers are as follows: RHO: MK209460 - MK209505; OPN1LW: MK209506 - MK209551; OPN1SW: MK209552 - MK209592. The GenBank numbers for the OPN1SW PCR sequences are MK248618 - MK248630. Gene alignments are available via Dryad (http://dx.doi.org/10.5061/dryad.456569k).
-
Gene alignment data from Multifactorial processes underlie parallel opsin loss in neotropical batsDryad Digital Repository, doi:10.5061/dryad.456569k.
Article and author information
Author details
Funding
National Science Foundation (1442142)
- Kalina TJ Davies
- Laurel R Yohe
- Stephen J Rossiter
National Science Foundation (1442314)
- Alexa Sadier
- Kun Yun
- Karen E Sears
National Science Foundation (1442278)
- Paul Donat
- Brandon P Hedrick
- Elizabeth R Dumont
European Research Council (310482)
- Kalina TJ Davies
- Stephen J Rossiter
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Patricia J Wittkopp, University of Michigan, United States
Ethics
Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to approved institutional animal care and use committee (IACUC) protocols 14199 at UIUC and 2017-093 at UCLA. Every effort was made to minimize suffering.
Version history
- Received: April 10, 2018
- Accepted: December 4, 2018
- Accepted Manuscript published: December 18, 2018 (version 1)
- Version of Record published: January 15, 2019 (version 2)
Copyright
© 2018, Sadier et al.
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.
Metrics
-
- 2,647
- views
-
- 347
- downloads
-
- 38
- 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)
Multifactorial processes underlie parallel opsin loss in neotropical bats
eLife 7:e37412.
https://doi.org/10.7554/eLife.37412
Further reading
-
- Evolutionary Biology
- Microbiology and Infectious Disease
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 ORFs, 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' 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.
-
- Evolutionary Biology
Extant ecdysozoans (moulting animals) are represented by a great variety of soft-bodied or articulated organisms that may or may not have appendages. However, controversies remain about the vermiform nature (i.e. elongated and tubular) of their ancestral body plan. We describe here Beretella spinosa gen. et sp. nov. a tiny (maximal length 3 mm) ecdysozoan from the lowermost Cambrian, Yanjiahe Formation, South China, characterized by an unusual sack-like appearance, single opening, and spiny ornament. Beretella spinosa gen. et sp. nov has no equivalent among animals, except Saccorhytus coronarius, also from the basal Cambrian. Phylogenetic analyses resolve both fossil species as a sister group (Saccorhytida) to all known Ecdysozoa, thus suggesting that ancestral ecdysozoans may have been non-vermiform animals. Saccorhytids are likely to represent an early off-shot along the stem-line Ecdysozoa. Although it became extinct during the Cambrian, this animal lineage provides precious insight into the early evolution of Ecdysozoa and the nature of the earliest representatives of the group.
