bioRxiv Science⌕ Search

Biology subjects

Murugesan, S. N.

Publications and source records attributed to Murugesan, S. N..

6 recordsLinked to original sources

A novel Hox gene promoter fuels the evolution of adaptive phenotypic plasticity

Adaptive phenotypic plasticity allows organisms to display distinct phenotypes in response to variable environments, but little is known about the genomic changes that promote the evolution of plasticity on a macroevolutionary scale. Combining spatial transcriptomics, comparative genomics, and genome editing, we show that temperature-mediated plasticity in the size of eyespot wing patterns in satyrid butterflies, a derived seasonal adaptation evolved [~]80 million years ago in this subfamily, is associated with the taxon-specific evolution of a novel promoter in the Hox gene Antennapedia (Antp). The promoter activates Antp expression specifically in satyrid eyespot center cells, sensitizes these cells to environmental temperatures, and plays a critical role in regulating satyrid eyespot size plasticity. Our study demonstrates that a taxon-specific cis-regulatory innovation in an ancestral developmental gene fueled the evolution of adaptive phenotypic plasticity across a clade of animals.

evolutionary biology↗

A micro-RNA drives a 100-million-year adaptive evolution of melanic patterns in butterflies and moths

In Lepidoptera (butterflies and moths), the genomic region around the gene cortex is a hotspot locus, repeatedly used to generate intraspecific melanic wing color polymorphisms across 100-million-years of evolution. However, the identity of the effector gene regulating melanic wing color within this locus remains unknown. Here, we show that none of the four candidate protein-coding genes within this locus, including cortex, serve as major effectors. Instead, a micro-RNA (miRNA), mir-193, serves as the major effector across three deeply diverged lineages of butterflies, and its function is conserved in Drosophila. In Lepidoptera, mir-193 is derived from a gigantic long non-coding RNA, ivory, and it functions by directly repressing multiple pigmentation genes. We show that a miRNA can drive repeated instances of adaptive evolution in animals.

genetics↗

Spatial and temporal regulation of Wnt signaling pathway members in the development of butterfly eyespots

Wnt signaling is involved in the differentiation of eyespot color patterns on the wings of butterflies, but the identity and spatio-temporal regulation of specific Wnt pathway members remains unclear. Here we explore the localization and function of armadillo/{beta}-catenin dependent (canonical) and armadillo/{beta}- catenin independent (non-canonical) Wnt signaling in eyespot development in Bicyclus anynana by localizing Armadillo (Arm), the expression of all seven wnt ligand and four frizzled receptor transcripts present in the genome of this species, and testing the function of arm and frizzled4 using CRISPR-Cas9. During mid to late larval wing development, Arm protein was present in cells at the center of the future eyespots, the foci, and the wing margin, but wnts expressed on the wing, wnt1 (wingless), wnt6, and wnt10 showed expression only some distance away from the foci, along the wing margin. The receptor frizzled9 was expressed in the wing margin and in finger-like projections leading to the foci during early larval wing development, overlapping in expression with Arm. At the same time, the receptor frizzled4 showed a novel expression pattern, anti-localized with Arm, where it is likely transducing non-canonical Wnt signaling. In the early pupal stage, wnt1 was newly expressed in the foci, as previously shown, along with Arm. In addition, frizzled4 and frizzled9-mediated Wnt signaling is likely repressing the expression of frizzled2, as these receptors have anti-colocalized expression domains. Arm had a conserved expression in three other nymphalid butterflies, and functional knockouts of arm and frizzled4 in B. anynana showed that both genes are essential for the differentiation of eyespots. These results show that distinct Wnt signaling pathways are essential for eyespot development in butterflies and are likely interacting to control their active domains.

developmental biology↗

The genetic basis of wing spots in Pieris canidia butterflies

Spots in pierid butterflies and eyespots in nymphalid butterflies are likely non-homologous wing colour pattern elements, yet they share a few features in common. Both develop black scales that depend on the function of the gene spalt, and both might have central signalling cells. This suggests that both pattern elements may be sharing common genetic circuitry. Hundreds of genes have already been associated with the development of nymphalid butterfly eyespot patterns, but the genetic basis of the simpler spot patterns on the wings of pierid butterflies has not been investigated. To facilitate studies of pierid wing patterns, we report a high-quality draft genome assembly for Pieris canidia, the Indian cabbage white. We then conducted transcriptomic analyses of pupal wing tissues sampled from the spot and non-spot regions of P. canidia at 3-6h post-pupation. A total of 1352 genes were differentially regulated between wing tissues with and without the black spot, including spalt, Kruppel-like factor 10, genes from the Toll, Notch, TGF-{beta}, and FGFR signalling pathways, and several genes involved in the melanin biosynthetic pathway. We identified 21 genes that are up-regulated in both pierid spots and nymphalid eyespots and propose that spots and eyespots share regulatory modules despite their likely independent origins.

evolutionary biology↗

Lepidopteran prolegs are novel traits, not leg homologs

Lepidopteran larvae have both thoracic legs and abdominal prolegs, yet it is unclear whether these are serial homologs. We examined the role of three Hox genes in proleg development in Bicyclus anynana butterflies using CRISPR-Cas9 and discovered that under a partial segment abdominal-A (abd-A) knockout, both types of appendages can develop in the same segment, arguing for prolegs being a novel trait, not a leg serial homolog. We also discover that specificity protein (sp) genes do not co-localize with Distal-less (Dll) in prolegs, as they do in legs, and that the proleg gene-regulatory network (GRN) mostly resembles the head-horn GRN, another novel trait in the lepidoptera. We propose that larval prolegs evolved from the co-option of a partial limb GRN into novel embryonic coordinates in the abdomen. One-Sentence SummaryThe chubby legs of caterpillars are evolutionary innovations

evolutionary biology↗

Butterfly eyespots evolved via co-option of the antennal gene-regulatory network

Butterfly eyespots are beautiful novel traits with an unknown developmental origin. Here we show that eyespots likely originated via co-option of the antennal gene-regulatory network (GRN) to novel locations on the wing. Using comparative transcriptome analysis, we show that eyespots cluster with antennae relative to multiple other tissues. Furthermore, three genes essential for eyespot development (Distal-less (Dll), spalt (sal), and Antennapedia (Antp)) share similar regulatory connections as those observed in the antennal GRN. CRISPR knockout of cis-regulatory elements (CREs) for Dll and sal led to the loss of eyespots and antennae, and also legs and wings, demonstrating that these CREs are highly pleiotropic. We conclude that eyespots likely re-used the ancient antennal GRN, a network previously implicated also in the development of legs and wings.

evolutionary biology↗