Discovering genomic and developmental mechanisms that underlie sensory innovations critical to adaptive diversification
2014-08-26


Liliana M. Dávalos
Professor of Conservation Biology
I’m interested in how biology and the environment shape biodiversity in time and space.
Related
- The Very Extended Phenotype: connecting genetics and evolution to ecological function
- Chance or necessity? Adaptive vs. non adaptive evolution in plant-frugivore interactions
- Uncovering skin immune proteins as predictors of resistance against WNS
- Diversification in Noctilionoid Bats
- Historical Biogeography of the Antilles
Publications
Comprising more than 1400 species, bats possess adaptations unique among mammals including powered flight, unexpected longevity given small body size, and extraordinary immunity. Some of the molecular mechanisms underlying these unique adaptations includes DNA repair, metabolism and immunity. However, analyses have been limited to a few divergent lineages, reducing the scope of inferences on gene family evolution across the Order Chiroptera. We conducted an exhaustive comparative genomic study of 37 bat species encompassing a large number of lineages, with a particular emphasis on multi-gene family evolution across immune system and metabolic genes. In agreement with previous analyses, we found lineage-specific expansions of the APOBEC3 and MHC-I gene families, and loss of the proinflammatory PYHIN gene family. We inferred more than 1,000 gene losses unique to bats, including genes involved in the regulation of inflammasome pathways such as epithelial defense receptors, the natural killer gene complex and the interferon-gamma induced pathway. Gene set enrichment analyses revealed genes lost in bats are involved in defense response against pathogen-associated molecular patterns and damage-associated molecular patterns. Gene family evolution and selection analyses indicate bats have evolved fundamental functional differences compared to other mammals in both innate and adaptive immune system, with the potential to enhance anti-viral immune response while dampening inflammatory signaling. In addition, metabolic genes have experienced repeated expansions related to convergent shifts to plant-based diets. Our analyses support the hypothesis that, in tandem with flight, ancestral bats had evolved a unique set of immune adaptations whose functional implications remain to be explored.
Diana Moreno Santillan,
Tanya Lama,
Yocelyn Gutiérrez Guerrero,
Alexis Brown,
Paul Donat,
Huabin Zhao,
Stephen Rossiter,
Laurel R. Yohe,
Joshua Potter,
Emma C. Teeling*,
Sonja Vernes,
Kalina T.J. Davies,
Eugene Myers,
Graham Hughes,
Zixia Huang,
Federico G. Hoffmann,
Angelique P. Corthals,
David Ray,
Liliana M. Dávalos
Bats possess extraordinary adaptations, including flight, echolocation, extreme longevity and unique immunity. High-quality genomes are crucial for understanding the molecular basis and evolution of these traits. Here we incorporated long-read sequencing and state-of-the-art scaffolding protocols1 to generate, to our knowledge, the first reference-quality genomes of six bat species (Rhinolophus ferrumequinum, Rousettus aegyptiacus, Phyllostomus discolor, Myotis myotis, Pipistrellus kuhlii and Molossus molossus). We integrated gene projections from our ‘Tool to infer Orthologs from Genome Alignments’ (TOGA) software with de novo and homology gene predictions as well as short- and long-read transcriptomics to generate highly complete gene annotations. To resolve the phylogenetic position of bats within Laurasiatheria, we applied several phylogenetic methods to comprehensive sets of orthologous protein-coding and noncoding regions of the genome, and identified a basal origin for bats within Scrotifera. Our genome-wide screens revealed positive selection on hearing-related genes in the ancestral branch of bats, which is indicative of laryngeal echolocation being an ancestral trait in this clade. We found selection and loss of immunity-related genes (including pro-inflammatory NF-κB regulators) and expansions of anti-viral APOBEC3 genes, which highlights molecular mechanisms that may contribute to the exceptional immunity of bats. Genomic integrations of diverse viruses provide a genomic record of historical tolerance to viral infection in bats. Finally, we found and experimentally validated bat-specific variation in microRNAs, which may regulate bat-specific gene-expression programs. Our reference-quality bat genomes provide the resources required to uncover and validate the genomic basis of adaptations of bats, and stimulate new avenues of research that are directly relevant to human health and disease1.
David Jebb,
Zixia Huang,
Martin Pippel,
Graham M. Hughes,
Ksenia Lavrichenko,
Paolo Devanna,
Sylke Winkler,
Lars S. Jermiin,
Emilia C. Skirmuntt,
Aris Katzourakis,
Lucy Burkitt-Gray,
David A. Ray,
Kevin A. M. Sullivan,
Juliana G. Roscito,
Bogdan M. Kirilenko,
Liliana M. Dávalos,
Angelique P. Corthals,
Megan L. Power,
Gareth Jones,
Roger D. Ransome,
Dina Dechmann,
Andrea G. Locatelli,
Sebastien J. Puechmaille,
Olivier Fedrigo,
Erich D. Jarvis,
Mark S. Springer,
Michael Hiller,
Sonja C. Vernes,
Eugene W. Myers,
Emma C. Teeling*