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Emx2 underlies the development and evolution of marsupial gliding membranes
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Journal Article
Emx2 underlies the development and evolution of marsupial gliding membranes
2024
Overview
Phenotypic variation among species is a product of evolutionary changes to developmental programs
1
,
2
. However, how these changes generate novel morphological traits remains largely unclear. Here we studied the genomic and developmental basis of the mammalian gliding membrane, or patagium—an adaptative trait that has repeatedly evolved in different lineages, including in closely related marsupial species. Through comparative genomic analysis of 15 marsupial genomes, both from gliding and non-gliding species, we find that the
Emx2
locus experienced lineage-specific patterns of accelerated
cis
-regulatory evolution in gliding species. By combining epigenomics, transcriptomics and in-pouch marsupial transgenics, we show that
Emx2
is a critical upstream regulator of patagium development. Moreover, we identify different
cis
-regulatory elements that may be responsible for driving increased
Emx2
expression levels in gliding species. Lastly, using mouse functional experiments, we find evidence that
Emx2
expression patterns in gliders may have been modified from a pre-existing program found in all mammals. Together, our results suggest that patagia repeatedly originated through a process of convergent genomic evolution, whereby regulation of
Emx2
was altered by distinct
cis
-regulatory elements in independently evolved species. Thus, different regulatory elements targeting the same key developmental gene may constitute an effective strategy by which natural selection has harnessed regulatory evolution in marsupial genomes to generate phenotypic novelty.
Patagia—the mammalian gliding membrane—repeatedly originated through a process of convergent genomic evolution, whereby the regulation of
Emx2
was altered by distinct
cis
-regulatory elements in independently evolved species.
Publisher
Nature Publishing Group UK,Nature Publishing Group
Subject
/ 13/51
/ 38/1
/ 38/109
/ 38/15
/ 38/23
/ 38/77
/ 38/91
/ Animals
/ Empty Spiracles Homeobox Proteins
/ Female
/ Gene Expression Regulation, Developmental
/ Genomes
/ Genomics
/ Gliding
/ Homeodomain Proteins - genetics
/ Homeodomain Proteins - metabolism
/ Humanities and Social Sciences
/ Humans
/ Male
/ Mammals
/ Marsupialia - anatomy & histology
/ Marsupialia - classification
/ Marsupialia - growth & development
/ Mice
/ Regulatory Sequences, Nucleic Acid - genetics
/ Science
/ Skin
/ Species
/ Transcription Factors - genetics
