Riccardo Papa

University of Puerto Rico at Río Piedras | UPR-RP · Department of Biology

Evolutionary variation in the wing pigmentation of butterflies and moths offers striking examples of adaptation by crypsis and mimicry. The cortex locus has been independently mapped as the locus controlling color polymorphisms in 15 lepidopteran species, suggesting that it acts as a genomic hotspot for the diversification of wing patterns, but fun...

Evolutionary variation in the wing pigmentation of butterflies and moths offers striking examples of adaptation by crypsis and mimicry. The cortex locus has been independently mapped as the locus controlling colour polymorphisms in 14 lepidopteran species, suggesting it acts as a genomic hotspot for the diversification of wing patterns, but functio...

Heliconius butterflies, a speciose genus of Müllerian mimics, represent a classic example of an adaptive radiation that includes a range of derived dietary, life history, physiological and neural traits. However, key lineages within the genus, and across the broader Heliconiini tribe, lack genomic resources, limiting our understanding of how adapti...

Butterfly color patterns provide visible and biodiverse phenotypic readouts of the patterning processes. While the secreted ligand WntA was shown to instruct the color pattern formation in butterflies, its mode of reception remains elusive. Butterfly genomes encode four homologues of the Frizzled-family of Wnt receptors. Here we show that CRISPR mo...

The recent increase in international fish trade leads to the need for improving the traceability of fishery products. In relation to this, consistent monitoring of the production chain focusing on technological developments, handling, processing and distribution via global networks is necessary. Molecular barcoding has therefore been suggested as t...

Little is known about the extent to which species use homologous regulatory architectures to achieve phenotypic convergence. By characterizing chromatin accessibility and gene expression in developing wing tissues, we compared the regulatory architecture of convergence between a pair of mimetic butterfly species. Although a handful of color pattern...

We reconstructed the SARS-CoV-2 epidemic caused by Omicron variant in Puerto Rico by sampling genomes collected during October 2021-May 2022. Our study revealed that Omicron BA.1 emerged and replaced Delta as the predominant variant in December 2021. Increased transmission rates and a dynamic landscape of Omicron sublineage infections followed.

Heliconius butterflies, a speciose genus of Müllerian mimics, represent a classic example of an adaptive radiation involving a range of derived dietary, life history, physiological and neural traits. However, key lineages within the genus, and across the broader Heliconiini tribe, lack genomic resources, contrasting our understanding of how adaptiv...

Neotropical Heliconius butterflies are well known for their intricate behaviors and multiple instances 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 functi...

Despite insertions and deletions being the most common structural variants (SVs) found across genomes, not much is known about how much these SVs vary within populations and between closely related species, nor their significance in evolution. To address these questions, we characterized the evolution of indel SVs using genome assemblies of three c...

Heliconius butterflies, a speciose genus of Müllerian mimics, represent a classic example of an adaptive radiation involving a range of derived dietary, life history, physiological and neural traits. However, key lineages within the genus, and across the broader Heliconiini tribe, lack genomic resources, contrasting our understanding of how adaptiv...

Background Puerto Rico has experienced the full impact of the COVID-19 pandemic. Since SARS-CoV-2, the virus that causes COVID-19, was first detected on the island in March of 2020, it spread rapidly though the island’s population and became a critical threat to public health. Methods We conducted a genomic surveillance study through a partnership...

Transcription factor (TF) DNA-binding specificity is determined by how their DNA-binding domain (DBD) interacts with DNA. TFs are identified by the sequence homology shared with described DBDs, which allows them to be classified into families. It is highly widely accepted that similar DBDs recognize similar DNA motifs. However, changes in a TF can...

Puerto Rico has experienced the full impact of the COVID-19 pandemic. Since SARS-CoV-2, the virus that causes COVID-19, was first detected on the island in March of 2020, it spread rapidly though the island’s population and became a critical threat to public health. We conducted a genomic surveillance study through a partnership with health agencie...

The evolution of mimicry in similarly defended prey is well described by the Müllerian mimicry theory, which predicts the convergence of warning patterns in order to gain the most protection from predators. However, despite this prediction, we can find great diversity of color patterns among Müllerian mimics such as Heliconius butterflies in the ne...

The evolution of mimicry in similarly defended prey is well described by Müllerian mimicry theory, which predicts the convergence of warning patterns in order to gain the most protection from predators. However, despite this prediction, we can find great diversity of color patterns amongst Müllerian mimics such as Heliconius butterflies in the neot...

The evolution of mimicry in similarly defended prey is well described by Müllerian mimicry theory, which predicts the convergence of warning patterns in order to gain the most protection from predators. However, despite this prediction, we can find great diversity of color patterns amongst Müllerian mimics such as Heliconius butterflies in the neot...

Heliconius himera reflecting its sister species H. erato (geographic color morph H. erato favorinus) from which it started diverging roughly 400 thousand years ago in Andean valleys of Ecuador and Peru.

Butterflies have become prominent models for studying the evolution and development of phenotypic variation. In Heliconius, extraordinary within species divergence and between species convergence in wing color patterns has driven decades of comparative genetic studies. However, connecting genetic patterns of diversification to the molecular mechani...

In Heliconius butterflies, wing colour pattern diversity and scale types are controlled by a few genes of large effect that regulate colour pattern switches between morphs and species across a large mimetic radiation. One of these genes, cortex, has been repeatedly associated with colour pattern evolution in butterflies. Here we carried out CRISPR...

Hybridizing species provide a powerful system to identify the processes that shape genomic variation and maintain species boundaries. However, complex histories of isolation, gene flow and selection often generate heterogeneous genomic landscapes of divergence that complicate reconstruction of the speciation history. Here, we explore patterns of di...

Many animal species remain separate not because their individuals fail to produce viable hybrids but because they "choose" not to mate. However, we still know very little of the genetic mechanisms underlying changes in these mate preference behaviours. Heliconius butterflies display bright warning patterns, which they also use to recognize conspeci...

Characterizing the genetic complexity of adaptation and trait evolution is a major emphasis of evolutionary biology and genetics. Incongruent findings from genetic studies have resulted in conceptual models ranging from a few large-effect loci to massively polygenic architectures. Here, we combine chromatin immunoprecipitation sequencing, Hi-C, RNA...

Müllerian mimicry strongly exemplifies the power of natural selection. However, the exact measure of such adaptive phenotypic convergence and the possible causes of its imperfection often remain unidentified. Here, we first quantify wing colour pattern differences in the forewing region of 14 co-mimetic colour pattern morphs of the butterfly specie...

Pictured is a postman butterfly (Heliconius melpomene rosina) perched on a leaf. Bas van Schooten, Jesyka Meléndez-Rosa, et al. uncovered sensory tissue gene-expression profiles in a pair of recently diverged butterfly species, H. melpomene rosina and Heliconius cydno chioneus, and identified candidate genes involved in chemical signal recognition,...

Wnt genes are major developmental genes highly conserved across all animals. Yet, our understanding of the Wnt gene repertoire and their functions is still largely incomplete. In Lepidoptera, Wnt genes have been implicated in wing pattern development. For example, WntA has been shown as a driver of wing pattern diversification in nymphalid butterfl...

Significance Insects are dependent on olfactory cues to complete biological processes, such as foraging, oviposition, and mate choice. While extensive experimental evidence supports the importance of chemical cues in these processes, genes involved in chemosensory integration of complex behavioral responses remain largely unknown. Using a combinati...

Characterizing the genetic architecture of species boundaries remains a difficult task. Hybridizing species provide a powerful system to identify the factors that shape genomic variation and, ultimately, identify the regions of the genome that maintain species boundaries. Unfortunately, complex histories of isolation, admixture and selection can ge...

A female Bicyclus anynana and an onlooking male. The dorsal eyespots display variation in number and are hidden from view on the inner sides of the wings. See Rivera-Colón et al., pp. 1059–1078. Image courtesy of William Piel and Antónia Monteiro.

Divergence in mating behaviors plays a major role during speciation, but we know little about the genetic mechanisms underlying the evolution of such traits. Reproductive isolation between the Neotropical butterflies Heliconius melpomene and H. cydno depends on shifts in mimetic warning patterns, which also act as mating cues. Preferences for consp...

Body plans often evolve through changes in the number of repeated parts or serial homologs. Using the butterfly Bicyclus anynana, RiveraColón et al. studied the genetics underlying heritability... The underlying genetic changes that regulate the appearance and disappearance of repeated traits, or serial homologs, remain poorly understood. One hypot...

Mullerian mimicry strongly exemplifies the power of natural selection. However, the exact measure of such adaptive phenotypic convergence and the possible causes of its imperfection often remain unidentified. The butterfly species Heliconius erato and Heliconius melpomene have a large diversity of co-mimicking geographic races with remarkable resem...

To what extent can we predict how evolution occurs? Do genetic architectures and developmental processes canalize the evolution of similar outcomes in a predictable manner? Or do historical contingencies impose alternative pathways to answer the same challenge? Examples of Müllerian mimicry between distantly related butterfly species provide natura...

Color pattern mimicry in Heliconius butterflies is a classic case study of complex trait adaptation via selection on a few large effect genes. Association studies have linked color pattern variation to a handful of noncoding regions, yet the presumptive cis-regulatory elements (CREs) that control color patterning remain unknown. Here we combine chr...

We used 20 de novo genome assemblies to probe the speciation history and architecture of gene flow in rapidly radiating Heliconius butterflies. Our tests to distinguish incomplete lineage sorting from introgression indicate that gene flow has obscured several ancient phylogenetic relationships in this group over large swathes of the genome. Introgr...

Butterfly eyes are complex organs that are composed of a diversity of proteins and they play a central role in visual signaling and ultimately, speciation and adaptation. Here, we utilized the whole eye transcriptome to obtain a more holistic view of the evolution of the butterfly eye while accounting for speciation events that co-occur with ancien...

The underlying genetic changes that regulate the appearance and disappearance of repeated traits, or serial homologs, remain poorly understood. One hypothesis is that variation in genomic regions flanking master regulatory genes, also known as input-output genes, controls variation in trait number, making the locus of evolution almost predictable....

OBJECTIVE Identifying the genomic changes that control morphological variation has major importance to understanding evolutionary change. Deep learning has the power to significantly improve the identification of complex genomic variation associated with morphological variation.

The underlying genetic changes that regulate the appearance and disappearance of repeated traits, or serial homologs, remain poorly understood. One hypothesis is that variation in genomic regions flanking master regulatory genes, also known as input-output genes, controls variation in trait number, making the locus of evolution almost predictable....

We here pioneer a low-cost assembly strategy for 20 Heliconiini genomes to characterize the evolutionary history of the rapidly radiating genus Heliconius. A bifurcating tree provides a poor fit to the data, and we therefore explore a reticulate phylogeny for Heliconius. We probe the genomic architecture of gene flow, and develop a new method to di...

Background Insects are the most diverse group of animals which have established intricate evolutionary interactions with bacteria. However, the importance of these interactions is still poorly understood. Few studies have focused on a closely related group of insect species, to test the similarities and differences between their microbiota. Helicon...

The biom file of the 38 butterflies

Number of reads and OTUs per butterfly species

The abundance of the three OTUs present in all samples Shown is their relative abundance to each other averaged over the different (sub)species.

The abundance of OTUs present in all samples for each of the 6 species and the two H. melpomene races Shown is their relative abundance to each other per butterfly.

The abundance of 4 microbial genera that showed significant abundance differences between species

T-test comparisons between phylogenetic diversity between female and male butterflies

Sex chromosomes are disproportionately involved in reproductive isolation and adaptation. In support of such a ‘large‐X’ effect, genome scans between recently diverged populations or species pairs often identify distinct patterns of divergence on the sex chromosome compared to autosomes. When measures of divergence between populations are higher on...

Sex chromosomes are disproportionately involved in reproductive isolation and adaptation. In support of such a ‘large-X’ effect, genome scans between recently diverged populations or species pairs often identify distinct patterns of divergence on the sex chromosome compared to autosomes. When measures of divergence between populations are higher on...

The use of image data to quantify, study and compare variation in the colors and patterns of organisms requires the alignment of images to establish homology, followed by color-based segmentation of images. Here we describe an R package for image alignment and segmentation that has applications to quantify color patterns in a wide range of organism...

Sex chromosomes are disproportionately involved in reproductive isolation and adaptation. In support of such a 'large X' effect, genome scans between recently diverged populations or species pairs often identify distinct patterns of divergence on the sex chromosome compared to autosomes. When measures of divergence between populations are higher on...

The use of image data to quantify, study and compare variation in the colours and patterns of organisms requires the alignment of images to establish homology, followed by colour‐based segmentation of images. Here, we describe an R package for image alignment and segmentation that has applications to quantify colour patterns in a wide range of orga...

The use of image data to quantify, study and compare variation in the colors and patterns of organisms requires the alignment of images to establish homology, followed by color-based segmentation of images. Here we describe an R package for image alignment and segmentation that has applications to quantify color patterns in a wide range of organism...

Identifying the genomic changes that control morphological variation and understanding how they generate diversity is a major goal of evolutionary biology. In Heliconius butterflies, a small number of genes control the development of diverse wing colour patterns. Here, we used full-genome sequencing of individuals across the Heliconius erato radiat...

We acknowledge the University of Puerto Rico, the Puerto Rico INBRE grant P20 GM103475 from the National Institute for General Medical Sciences (NIGMS), a component of the National Institutes of Health (NIH); CNRS Nouraugues and CEBA awards (B.A.C.); National Science Foundation awards DEB-1257839 (B.A.C.), DEB-1257689 (W.O.M.), DEB-1027019 (W.O.M.)...

In a world of chemical cues, smell and taste are essential senses for survival. Here we focused on Heliconius, a diverse group of butterflies that exhibit variation in pre- and post-zygotic isolation and chemically-mediated behaviors across their phylogeny. Our study examined the ionotropic receptors, a recently discovered class of receptors that a...

A key to understanding the origins of species is determining the evolutionary processes that drive the patterns of genomic divergence during speciation. New genomic technologies enable the study of high-resolution genomic patterns of divergence across natural speciation continua, where taxa pairs with different levels of reproductive isolation can...

Wing-pattern mimicry in butterflies has provided an important example of adaptation since Charles Darwin and Alfred Russell Wallace proposed evolution by natural selection >150 years ago. The neotropical butterfly genus Heliconius played a central role in the development of mimicry theory and has since been studied extensively in the context of eco...

Hybrid zones can be valuable tools for studying evolution and identifying genomic regions responsible for adaptive divergence and underlying phenotypic variation. Hybrid zones between subspecies of Heliconius butterflies can be very narrow and are maintained by strong selection acting on colour pattern. The co-mimetic species H. erato and H. melpom...

The lionfish (Pterois volitans), has become an abundant alien species along the southeast coast of the United States of America and in Caribbean coastal waters. Although, they represent a major concern in conservation, no studies have yet assessed their population ecology and genetic structure simultaneously. We collected 227 lionfish from 24 sites...

Fueled by new technologies that allow rapid and inexpensive assessment of fine scale individual genomic variation, researchers are making transformational discoveries at the interface between genomes and biological complexity. Here we review genomic research in Heliconius butterflies - a radiation characterized by extraordinary phenotypic diversity...

Hybrid zones can be valuable tools for studying evolution and identifying genomic regions responsible for adaptive divergence and underlying phenotypic variation. Hybrid zones between subspecies of Heliconius butterflies can be very narrow and are maintained by strong selection acting on colour pattern. The co-mimetic species H. erato and H. melpom...

A fish population of the carp family Cyprinidae with atypical phenotypic characteristics was observed in one of the main catchments of the Pollino National Park, a valuable, protected area in southern Italy. In this area, the Italian roach Rutilus rubilio (Bonaparte, 1837), a native endemic fish of Tyrrhenean regions, has been introduced in sympatr...

Recent studies indicate that relatively few genomic regions are repeatedly involved in the evolution of Heliconius butterfly wing patterns. Although this work demonstrates a number of cases where homologous loci underlie both convergent and divergent wing pattern change among different Heliconius species, it is still unclear exactly how many loci u...

Co-dominant and gene based markers. Information of co-dominant and gene based markers used respectively for linkage analysis and fine scale mapping of the D color pattern gene interval. Primers sequence and reference article in which the loci have been developed is reported together with locus ID and linkage information. (JPG)

Anchors AFLP loci. Anchors AFLP loci. AFLP markers isolated and sequenced across our collection of crosses and their relative nucleotide composition are shown. Provenance of allele and characteristic (MI = Male Informative; FI = Female Informative; BI = Both Informative parents) is reported. (JPG)

Color spectrum and absorbance. A) Area of the wing measured by a spectrophotometer to distinguish between the amount of white and yellow pigment. B) From right to left the typical absorbance spectrums for individuals that were fully white, yellow, or red is presented. (TIF)

Overall QTL analysis for the forewing Big-Spot (BS) size variation. Overall QTL analysis for shape in the forewing Big-Spot (BS) showing chromosomes on which QTLs were found. Only those QTLs with probabilities smaller than 0.01 of occurring by chance were considered significant, and were included in additional analyses. LG = linkage group; marker =...

Size analysis. A and B represent the location of landmarks used for quantitative measure of band size variation in the forewing Big-Spot (BS) and Not-Spot (NS) in a simplified butterfly's wing cartoon and real sample respectively. Functions used for calculations of areas were: WingSpot = abs((x3*y10−x10*y3+x10*y11−x11*y10+x11*y12−x12*y11+x12*y13−x1...