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).
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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.
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.
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.
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Multifactorial processes underlie parallel opsin loss in neotropical bats
eLife 7:e37412.
https://doi.org/10.7554/eLife.37412
Further reading
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- Evolutionary Biology
The majority of highly polymorphic genes are related to immune functions and with over 100 alleles within a population, genes of the major histocompatibility complex (MHC) are the most polymorphic loci in vertebrates. How such extraordinary polymorphism arose and is maintained is controversial. One possibility is heterozygote advantage (HA), which can in principle maintain any number of alleles, but biologically explicit models based on this mechanism have so far failed to reliably predict the coexistence of significantly more than 10 alleles. We here present an eco-evolutionary model showing that evolution can result in the emergence and maintenance of more than 100 alleles under HA if the following two assumptions are fulfilled: first, pathogens are lethal in the absence of an appropriate immune defence; second, the effect of pathogens depends on host condition, with hosts in poorer condition being affected more strongly. Thus, our results show that HA can be a more potent force in explaining the extraordinary polymorphism found at MHC loci than currently recognised.
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As pathogens spread in a population of hosts, immunity is built up, and the pool of susceptible individuals are depleted. This generates selective pressure, to which many human RNA viruses, such as influenza virus or SARS-CoV-2, respond with rapid antigenic evolution and frequent emergence of immune evasive variants. However, the host’s immune systems adapt, and older immune responses wane, such that escape variants only enjoy a growth advantage for a limited time. If variant growth dynamics and reshaping of host-immunity operate on comparable time scales, viral adaptation is determined by eco-evolutionary interactions that are not captured by models of rapid evolution in a fixed environment. Here, we use a Susceptible/Infected model to describe the interaction between an evolving viral population in a dynamic but immunologically diverse host population. We show that depending on strain cross-immunity, heterogeneity of the host population, and durability of immune responses, escape variants initially grow exponentially, but lose their growth advantage before reaching high frequencies. Their subsequent dynamics follows an anomalous random walk determined by future escape variants and results in variant trajectories that are unpredictable. This model can explain the apparent contradiction between the clearly adaptive nature of antigenic evolution and the quasi-neutral dynamics of high-frequency variants observed for influenza viruses.
