The diversification of butterfly wing patterns: progress and prospects.

Butterfly wings display rich phenotypic diversity and are associated with complex biological functions, thus serving as an important evolutionary system to address the genetic basis and evolution of phenotypic diversification. We review recent butterfly studies that revealed complex functions underlying diversified wing patterns and describe the genetic and environmental factors involved in wing pattern determinations. These factors lead to inter-specific divergence, genetic polymorphism, and phenotypic plasticity, which in many cases are decided by several key genes. We also summarize the research advances on gene co-option as an important origin of functional complexity and evolutionary novelty. These findings reveal a pattern of evolutionary innovation within a constrained developmental framework during butterfly wing morphogenesis, but further research is required to gain a systematic and comprehensive understanding.

The evolution and diversification of oakleaf butterflies.

Oakleaf butterflies in the genus Kallima have a polymorphic wing phenotype, enabling these insects to masquerade as dead leaves. This iconic example of protective resemblance provides an interesting evolutionary paradigm that can be employed to study biodiversity. We integrated multi-omic data analyses and functional validation to infer the evolutionary history of Kallima species and investigate the genetic basis of their variable leaf wing patterns. We find that Kallima butterflies diversified in the eastern Himalayas and dispersed to East and Southeast Asia. Moreover, we find that leaf wing polymorphism is controlled by the wing patterning gene cortex, which has been maintained in Kallima by long-term balancing selection. Our results provide macroevolutionary and microevolutionary insights into a model species originating from a mountain ecosystem.

Atypical laminin spots and pull-generated microtubule-actin projections mediate Drosophila wing adhesion.

During Drosophila metamorphosis, dorsal and ventral wing surfaces adhere, separate, and reappose in a paradoxical process involving cell-matrix adhesion, matrix production and degradation, and long cellular projections. The identity of the intervening matrix, the logic behind the adhesion-reapposition cycle, and the role of projections are unknown. We find that laminin matrix spots devoid of other main basement membrane components mediate wing adhesion. Through live imaging, we show that long microtubule-actin cables grow from those adhesion spots because of hydrostatic pressure that pushes wing surfaces apart. Formation of cables resistant to pressure requires spectraplakin, Patronin, septins, and Sdb, a SAXO1/2 microtubule stabilizer expressed under control of wing intervein-selector SRF. Silkworms and dead-leaf butterflies display similar dorso-ventral projections and expression of Sdb in intervein SRF-like patterns. Our study supports the morphogenetic importance of atypical basement-membrane-related matrices and dissects matrix-cytoskeleton coordination in a process of great evolutionary significance.

Using comprehensive machine-learning models to classify complex morphological characters.

Recognizing and classifying multiple morphological features, such as patterns, sizes, and textures, can provide a comprehensive understanding of their variability and phenotypic evolution. Yet, quantitatively measuring complex morphological characters remains challenging.We provide a machine learning-based pipeline (SVMorph) to consider and classify complex morphological characters in multiple organisms that have either small or large datasets.Our pipeline integrates two descriptors, histogram of oriented gradient and local binary pattern, to meet various classification needs. We also optimized feature extraction by adding image data augmentation to improve model generalizability.We tested SVMorph on two real-world examples to demonstrate that it can be used with small training datasets and limited computational resources. Comparing with multiple CNN-based methods and traditional techniques, we show that SVMorph is reliable and fast in texture-based individual classification. Thus, SVMorph can be used to efficiently classify multiple morphological characters in distinct nonmodel organisms.

A widely diverged locus involved in locomotor adaptation in Heliconius butterflies.

Heliconius butterflies have undergone adaptive radiation and therefore serve as an excellent system for exploring the continuum of speciation and adaptive evolution. However, there is a long-lasting paradox between their convergent mimetic wing patterns and rapid divergence in speciation. Here, we characterize a locus that consistently displays high divergence among Heliconius butterflies and acts as an introgression hotspot. We further show that this locus contains multiple genes related to locomotion and conserved in Lepidoptera. In light of these findings, we consider that locomotion traits may be under selection, and if these are heritable traits that are selected for, then they might act as species barriers.