Biology subjects

Shapiro, M. D.

Publications and source records attributed to Shapiro, M. D..

14 recordsLinked to original sources

bioRxiv2025

Widespread variation in EDNRB2 is associated with diverse melanin loss phenotypes across avian species

Plumage pigmentation plays critical roles in survival and reproductive success in birds, from providing camouflage and thermoregulation to mediating elaborate mating displays. The genetic and developmental origins of diverse plumage pigmentation patterns remain incompletely understood in part due to limited intraspecific variation and high levels of genetic divergence between distantly related species. Domestic avian species are more tractable models for understanding the genetic architecture of plumage pigmentation, but the relevance of domestic phenotypes to plumage patterns observed in the wild is not clear. Here, we used comparative genomic approaches to examine coding variation in EDNRB2, a candidate gene associated with loss of plumage melanin in several species, in representative genomes from a diverse array of wild and domestic birds. We found widespread coding variation in EDNRB2 and in other pigmentation genes with limited pleiotropic roles in development. We also found that EDNRB2- mediated melanin loss may play a critical role in establishing bright non-melanin plumage colors. This work highlights EDNRB2 as a key candidate gene for mediating the development of both interspecific and intraspecific plumage variation and demonstrates the applicability of findings in domestic species to understanding avian plumage patterning more broadly.

genetics↗

bioRxiv2023

Assembly and annotation of two high-quality columbid reference genomes from sequencing of a Columba livia x Columba guinea F1 hybrid

Pigeons and doves (family Columbidae) are one of the most diverse extant avian lineages, and many species have served as key models for evolutionary genomics, developmental biology, physiology, and behavioral studies. Building genomic resources for colubids is essential to further many of these studies. Here, we present high-quality genome assemblies and annotations for two columbid species, Columba livia and C. guinea. We simultaneously assembled C. livia and C. guinea genomes from long-read sequencing of a single F1 hybrid individual. The new C. livia genome assembly (Cliv_3) shows improved completeness and contiguity relative to Cliv_2.1, with an annotation incorporating long-read IsoSeq data for more accurate gene models. Intensive selective breeding of C. livia has given rise to hundreds of breeds with diverse morphological and behavioral characteristics, and Cliv_3 offers improved tools for mapping the genomic architecture of interesting traits. The C. guinea genome assembly is the first for this species and is a new resource for avian comparative genomics. Together, these assemblies and annotations provide improved resources for functional studies of columbids and avian comparative genomics in general. ARTICLE SUMMARYPigeons and doves are important models for evolutionary genomics, developmental biology, physiology, and behavioral studies. Here, we present high-quality reference genome assemblies and annotations for two pigeon species, the domestic rock pigeon (Columba livia) and the African speckled pigeon (C. guinea). These assemblies and annotations provide improved resources for both comparative genomics and functional studies.

genomics↗

bioRxiv2021

Long-distance dispersal of pigeons and doves generated new ecological opportunities for host-switching and adaptive radiation by their parasites

Adaptive radiation is an important mechanism of organismal diversification, and can be triggered by new ecological opportunities. Although poorly studied in this regard, parasites present an ideal system to study adaptive radiations because of their close associations with host species. Both experimental and comparative studies suggest that the ectoparasitic wing lice of pigeons and doves have undergone an adaptive radiation, resulting in differences in both body size and overall coloration. Here we show that long-distance dispersal by dove hosts was important for parasite diversification, providing new ecological opportunities for parasites to speciate by host-switching. We further show that these new opportunities for host-switching decreased over time, and cospeciation became the more dominant mode of parasite speciation. Taken together, our results suggest that host dispersal, followed by host-switching, provided novel ecological opportunities that facilitated adaptive radiation by parasites.

evolutionary biology↗

bioRxiv2021

Complex genetic architecture of three-dimensional craniofacial shape variation in domestic pigeons

Deciphering the genetic basis of vertebrate craniofacial variation is a longstanding biological problem with broad implications in evolution, development, and human pathology. One of the most stunning examples of craniofacial diversification is the adaptive radiation of birds, in which the beak serves essential roles in virtually every aspect of their life histories. The domestic pigeon (Columba livia) provides an exceptional opportunity to study the genetic underpinnings of craniofacial variation because of its unique balance of experimental accessibility and extraordinary phenotypic diversity within a single species. We used traditional and geometric morphometrics to quantify craniofacial variation in an F2 laboratory cross derived from the straight-beaked Pomeranian Pouter and curved-beak Scandaroon pigeon breeds. Using a combination of genome-wide quantitative trait locus scans and multi-locus modeling, we identified a set of genetic loci associated with complex shape variation in the craniofacial skeleton, including beak curvature, braincase shape, and mandible shape. Some of these loci control coordinated changes between different structures, while others explain variation in the size and shape of specific skull and jaw regions. We find that in domestic pigeons, a complex blend of both independent and coupled genetic effects underlie three-dimensional craniofacial morphology.

genetics↗

bioRxiv2021

A ROR2 coding variant is associated with craniofacial variation in domestic pigeons

Vertebrate craniofacial morphogenesis is a highly orchestrated process that is directed by evolutionarily conserved developmental pathways 1,2. Within species, canalized developmental programs typically produce only modest morphological variation. However, as a result of millennia of artificial selection, the domestic pigeon (Columba livia) displays radical variation in craniofacial morphology within a single species. One of the most striking cases of pigeon craniofacial variation is the short beak phenotype, which has been selected in numerous breeds. Classical genetic experiments suggest that pigeon beak length is regulated by a small number of genetic factors, one of which is sex-linked (Ku2 locus) 3-5. However, the molecular genetic underpinnings of pigeon craniofacial variation remain unknown. To determine the genetic basis of the short beak phenotype, we used geometric morphometrics and quantitative trait loci (QTL) mapping on an F2 intercross between a short-beaked Old German Owl (OGO) and a medium-beaked Racing Homer (RH). We identified a single locus on the Z-chromosome that explains a majority of the variation in beak morphology in the RH x OGO F2 population. In complementary comparative genomic analyses, we found that the same locus is also strongly differentiated between breeds with short and medium beaks. Within the differentiated Ku2 locus, we identified an amino acid substitution in the non-canonical Wnt receptor ROR2 as a putative regulator of pigeon beak length. The non-canonical Wnt (planar cell polarity) pathway serves critical roles in vertebrate neural crest cell migration and craniofacial morphogenesis 6,7. In humans, homozygous ROR2 mutations cause autosomal recessive Robinow syndrome, a rare congenital disorder characterized by skeletal abnormalities, including a widened and shortened facial skeleton 8,9. Our results illustrate how the extraordinary craniofacial variation among pigeons can reveal genetic regulators of vertebrate craniofacial diversity.

genetics↗

bioRxiv2021

Two Genomic Loci Control Three Eye Colors in the Domestic Pigeon (Columba livia)

The iris of the eye shows striking color variation across vertebrate species, and may play important roles in crypsis and communication. The domestic pigeon (Columba livia) has three common iris colors, orange, pearl (white), and bull (dark brown), segregating in a single species, thereby providing a unique opportunity to identify the genetic basis of iris coloration. We used comparative genomics and genetic mapping in laboratory crosses to identify two candidate genes that control variation in iris color in domestic pigeons. We identified a nonsense mutation in the solute carrier SLC2A11B that is shared among all pigeons with pearl eye color, and a locus associated with bull eye color that includes EDNRB2, a gene involved in neural crest migration and pigment development. However, bull eye is likely controlled by a heterogeneous collection of alleles across pigeon breeds. We also found that the EDNRB2 region is associated with regionalized plumage depigmentation (piebalding). Our results establish a genetic link between iris and plumage color, two traits that were long known by pigeon breeders to co-occur, and demonstrate the importance of gene duplicates in establishing possibilities and constraints in the evolution of color and color pattern among vertebrates.

genetics↗

bioRxiv2021

Trio-binned genomes of the woodrats Neotoma bryanti and N. lepida reveal novel gene islands and rapid copy number evolution of xenobiotic metabolizing cytochrome p450 genes

The genomic architecture underlying the origins and maintenance of biodiversity is an increasingly accessible feature of species, due in large part to third-generation sequencing and novel analytical toolsets. Woodrats of the genus Neotoma provide a unique opportunity to study how vertebrate herbivores respond to climate change, as two sister species (N. bryanti and N. lepida) independently achieved a major dietary feat - switching to the novel and toxic food source creosote bush (Larrea tridentata) - in the aftermath of a natural warming event. To better understand the genetic mechanisms underlying this ability, we employed a trio binning sequencing approach with a N. bryanti x N. lepida F1 hybrid, resulting in phased, chromosome-level, highly complete, haploid genome assemblies for each species from one individual. Using these new assemblies, we explored the genomic architecture of three cytochrome p450 subfamilies (2A, 2B, and 3A) that play key roles in the metabolism of naturally occurring toxic dietary compounds. We found that woodrats show expansions of all three p450 gene families, including the evolution of multiple novel gene islands within the 2B and 3A subfamilies. Our assemblies demonstrate that trio binning from an F1 hybrid rodent effectively recovers parental genomes from species that diverged more than a million years ago. Turnover and novelty in detoxification gene islands in herbivores is widespread within distinct p450 subfamilies, and may have provided the crucial substrate for dietary adaptation during environmental change.

genomics↗

bioRxiv2020

The Almond plumage color pattern is associated with eye pigmentation defects in the domestic pigeon (Columba livia)

Changes in epidermal pigmentation are associated with eye defects in humans and other vertebrates. In the rock pigeon (Columba livia), the sex-linked Almond color pattern is characterized by hypopigmentation of epidermal structures. The trait is controlled by the classical Stipper (St) locus, and homozygous (ZStZSt) Almond males often have severe eye defects. Heterozygous (ZStZ+) and hemizygous (ZStW) pigeons do not typically have obvious eye defects, suggesting that higher dosage of the mutant allele is deleterious. Because Almond pigeons have pronounced hypopigmentation in epidermal structures, we hypothesized that they might also have reduced eye pigmentation. Here, we examined pigmentation in the iris, ciliary body, anterior retinal pigmented epithelium (RPE), and posterior RPE in pigeons with and without Almond alleles. We found that pigmentation of anterior segment structures was reduced in birds with at least one Almond allele. However, posterior eye pigmentation was substantially reduced only in homozygous Almond birds. We postulate that the gradient of effects on eye pigmentation is due to the different embryological origins of anterior and posterior eye pigment-producing cells.

developmental biology↗

bioRxiv2020

The assembled and annotated genome of the pigeon louse Columbicola columbae, a model ectoparasite

The pigeon louse Columbicola columbae is a longstanding and important model for studies of ectoparasitism and host-parasite coevolution. However, a deeper understanding of its evolution and capacity for rapid adaptation is limited by a lack of genomic resources. Here, we present a high-quality draft assembly of the C. columbae genome, produced using a combination of Oxford Nanopore, Illumina, and Hi-C technologies. The final assembly is 208 Mb in length, with 12 chromosome-size scaffolds representing 98.1% of the assembly. For gene model prediction, we used a novel clustering method (wavy_choose) for Oxford Nanopore RNA-seq reads to feed into the MAKER annotation pipeline. High recovery of conserved single-copy orthologs (BUSCOs) suggests that our assembly and annotation are both highly complete and highly accurate. Consistent with the results of the only other assembled louse genome, Pediculus humanus, we find that C. columbae has a relatively low density of repetitive elements, the majority of which are DNA transposons. Also similar to P. humanus, we find a reduced number of genes encoding opsins, G protein-coupled receptors, odorant receptors, insulin signaling pathway components, and detoxification proteins in the C. columbae genome, relative to other insects. We propose that such losses might characterize the genomes of obligate, permanent ectoparasites with predictable habitats, limited foraging complexity, and simple dietary regimes. The sequencing and analysis for this genome were relatively low-cost, and took advantage of a new clustering technique for Oxford Nanopore RNAseq reads that will be useful to future genome projects.

genomics↗

bioRxiv2019

A copy number variant is associated with a spectrum of pigmentation patterns in the rock pigeon (Columba livia)

Rock pigeons (Columba livia) display an extraordinary array of pigment pattern variation. One such pattern, Almond, is characterized by a variegated patchwork of plumage colors that are distributed in an apparently random manner. Almond is a sex-linked, semi-dominant trait controlled by the classical Stipper (St) locus. Heterozygous males (ZStZ+ sex chromosomes) and hemizygous Almond females (ZStW) are favored by breeders for their attractive plumage. In contrast, homozygous Almond males (ZStZSt) develop severe eye defects and lack all plumage pigmentation, suggesting that higher dosage of the mutant allele is deleterious. To determine the molecular basis of Almond, we compared the genomes of Almond pigeons to non-Almond pigeons and identified a candidate St locus on the Z chromosome. We found a copy number variant (CNV) within the differentiated region that captures complete or partial coding sequences of four genes, including the melanosome maturation gene Mlana. We did not find fixed coding changes in genes within the CNV, but all genes are misexpressed in regenerating feather bud collar cells of Almond birds. Notably, six other alleles at the St locus are associated with depigmentation phenotypes, and all exhibit expansion of the same CNV. Structural variation at St is linked to diversity in plumage pigmentation and gene expression, and thus provides a potential mode of rapid phenotypic evolution in pigeons.\n\nAUTHOR SUMMARYThe genetic changes responsible for different animal color patterns are poorly understood, due in part to a paucity of research organisms that are both genetically tractable and phenotypically diverse. Domestic pigeons (Columba livia) have been artificially selected for many traits, including an enormous variety of color patterns that are variable both within and among different breeds of this single species. We investigated the genetic basis of a sex-linked color pattern in pigeons called Almond that is characterized by a sprinkled pattern of plumage pigmentation. Pigeons with one copy of the Almond allele have desirable color pattern; however, male pigeons with two copies of the Almond mutation have severely depleted pigmentation and congenital eye defects. By comparing the genomes of Almond and non-Almond pigeons, we discovered that Almond pigeons have extra copies of a chromosome region that contains a gene that is critical for the formation of pigment granules. We also found that different numbers of copies of this region are associated with varying degrees of pigment reduction. The Almond phenotype in pigeons bears a remarkable resemblance to Merle coat color mutants in dogs, and our new results from pigeons suggest that similar genetic mechanisms underlie these traits in both species. Our work highlights the role of gene copy number variation as a potential driver of rapid phenotypic evolution.

genetics↗

bioRxiv2019

Pigeon foot feathering reveals conserved limb identity networks

The tetrapod limb is a stunning example of evolutionary diversity, with dramatic variation not only among distantly related species, but also between the serially homologous forelimbs (FLs) and hindlimbs (HLs) within species. Despite this variation, highly conserved genetic and developmental programs underlie limb development and identity in all tetrapods, raising the question of how limb diversification is generated from a conserved toolkit. In some breeds of domestic pigeon, shifts in the expression of two conserved limb identity transcription factors, PITX1 and TBX5, are associated with the formation of feathered HLs with partial FL identity. To determine how modulation of PITX1 and TBX5 expression affects downstream gene expression, we compared the transcriptomes of embryonic limb buds from pigeons with scaled and feathered HLs. We identified a set of differentially expressed genes enriched for genes encoding transcription factors, extracellular matrix proteins, and components of developmental signaling pathways with important roles in limb development. A subset of the genes that distinguish scaled and feathered HLs are also differentially expressed between FL and scaled HL buds in pigeons, pinpointing a set of gene expression changes downstream of PITX1 and TBX5 in the partial transformation from HL to FL identity. We extended our analyses by comparing pigeon limb bud transcriptomes to chicken, anole lizard, and mammalian datasets to identify deeply conserved PITX1- and TBX5-regulated components of the limb identity program. Our analyses reveal a suite of predominantly low-level gene expression changes that are conserved across amniotes to regulate the identity of morphologically distinct limbs.\n\nSummary statementIn feather-footed pigeons, mutant alleles of PITX1 and TBX5 drive the partial redeployment of an evolutionarily conserved forelimb genetic program in the hindlimb.

developmental biology↗

bioRxiv2018

Experimental evolution of reproductive isolation from a single natural population

Ecological speciation occurs when local adaptation generates reproductive isolation as a by-product of natural selection1-3. Although ecological speciation is a fundamental source of diversification, the mechanistic link between natural selection and reproductive isolation remains poorly understood, especially in natural populations2-6. Here we show that experimental evolution of parasite body size over four years (ca. 60 generations) leads to reproductive isolation in natural populations of feather lice on birds. When lice are transferred to pigeons of different sizes they rapidly evolve differences in body size that are correlated with host size. These size differences trigger mechanical mating isolation between lice that are locally adapted to the different sized hosts. Size differences among lice also influence the outcome of competition between males for access to females. Thus, body size directly mediates reproductive isolation through its influence on both inter-sexual compatibility and intra-sexual competition. Our results confirm that divergent natural selection acting on a single phenotypic trait can cause reproductive isolation to emerge from a single natural population in real time.

evolutionary biology↗

bioRxiv2018

Host defense triggers rapid adaptive radiation in experimentally evolving parasites

Adaptive radiation occurs when the members of a single lineage evolve different adaptive forms in response to selection imposed by competitors or predators. Iconic examples include Darwins finches, Caribbean anoles, and Hawaiian silverswords, all of which live on islands. Parasites, which live on host \"islands,\" show macroevolutionary patterns consistent with adaptive radiation in response to host-imposed selection. Here we show rapid adaptive divergence of experimentally evolving feather lice in response to preening, the main host defense. We demonstrate that host defense exerts strong phenotypic selection for crypsis in lice transferred to different colored rock pigeons (Columba livia). During four years of experimental evolution ([~]60 generations), the lice evolved heritable differences in color. The color differences spanned the phenotypic distribution of congeneric species of lice adapted to other species of pigeons. Our results indicate that host-mediated selection triggers rapid divergence in the adaptive radiation of parasites, which are among the most diverse organisms on earth. Our research suggests that host defense should be included with competition and predation as a major mechanism driving the evolution of biodiversity by adaptive radiation.

evolutionary biology↗

bioRxiv2017

Improved genome assembly and annotation for the rock pigeon (Columba livia)

The domestic rock pigeon (Columba livia) is among the most widely distributed and phenotypically diverse avian species. This species is broadly studied in ecology, genetics, physiology, behavior, and evolutionary biology, and has recently emerged as a model for understanding the molecular basis of anatomical diversity, the magnetic sense, and other key aspects of avian biology. Here we report an update to the C. livia genome reference assembly and gene annotation dataset. Greatly increased scaffold lengths in the updated reference assembly, along with an updated annotation set, provide improved tools for evolutionary and functional genetic studies of the pigeon, and for comparative avian genomics in general.

genomics↗