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Early stages of butterfly speciation are associated with widespread gene expression divergence in sensory tissues


Authors:
Ningning Wu 1; Steven Van Belleghem 2; Brian Counterman 3; Riccardo Papa 2,4; Wei Zhang 1,5

Affiliations:
1) State Key Laboratory of Protein and Plant Gene Research, School of Life Sciences, Peking University, Beijing 100871, China; 2) Department of Biology, University of Puerto Rico, Rio Piedras, San Juan 00925, Puerto Rico, United States of America; 3) Department of Biological Sciences, Auburn University, Auburn, AL 36849, United States of America; 4) Molecular Sciences and Research Center, University of Puerto Rico, San Juan 00907, Puerto Rico, United States of America; 5) Peking-Tsinghua Center for Life Sciences, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing 100871, China

Keywords:
Speciation & hybridization

Neotropical Heliconius butterflies are well-known for their intricate behaviors and multiple examples of incipient speciation. Chemosensing plays a fundamental role in the life history of these groups of butterflies and in the establishment of reproductive isolation. However, chemical communication involves synergistic sensory and accessory functions, and it remains challenging to investigate the molecular underpinnings that result in behavioral differences. Here, we examine the gene expression profiles and genomic divergence of three sensory tissues (antennae, legs, and mouth parts), across sexes (females and males) and life stages (mated and unmated females) in two hybridizing butterflies, Heliconius melpomene and Heliconius cydno. By integrating comparative transcriptomic and population genomic approaches, we found evidence of widespread gene expression divergence that supports a crucial role of sensory tissues in the establishment of species barriers. Our work strongly supports the unique chemosensory function of antennae, the importance of the Z chromosome in interspecific divergence, and the nonnegligible role of non-chemosensory genes in the divergence of chemosensory tissues. Collectively, our study contributes to a better understanding of the genetic basis of chemosensory mechanisms promoting reproductive isolation and speciation.