Biology subjects

Van Belleghem, S. M.

Publications and source records attributed to Van Belleghem, S. M..

12 recordsLinked to original sources

bioRxiv2024

Genetic basis of an adaptive polymorphism controlling butterfly silver iridescence

Identifying the genes and mutations that drive phenotypic variation and which are subject to selection is crucial for understanding evolutionary processes. Mormon Fritillary butterflies (Speyeria mormonia) exhibit a striking wing color polymorphism throughout their range: typical morphs bear silver spots on their ventral surfaces, and can co-occur with unsilvered morphs displaying a dull coloration1. Through genome-wide association studies in two polymorphic populations, we fine-map this difference in silvering to the 3 region of the transcription factor gene optix. The expression of optix is confined to the unsilvered regions that surround the spots, and these patterns are transformed to a silver identity upon optix RNAi knockdown, implicating optix as a repressor of silver scales in this butterfly. We show that the unsilvered optix haplotype shows signatures of recent selective sweeps, and that this allele is shared with the monomorphic, unsilvered species Speyeria hydaspe, suggesting that introgressions facilitate the exchange of variants of adaptive potential across species. Remarkably, these findings parallel the role of introgressions and cis-regulatory modulation of optix in shaping the aposematic red patterns of Heliconius butterflies2-7, a lineage that separated from Speyeria 45 million years ago8. The genetic basis of adaptive variation can thus be more predictable than often presumed, even for traits that appear divergent across large evolutionary distances. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=199 SRC="FIGDIR/small/628425v1_ufig1.gif" ALT="Figure 1"> View larger version (112K): org.highwire.dtl.DTLVardef@5d2a9borg.highwire.dtl.DTLVardef@982c74org.highwire.dtl.DTLVardef@8e90b3org.highwire.dtl.DTLVardef@1bddf3c_HPS_FORMAT_FIGEXP M_FIG Graphical Abstract C_FIG

evolutionary biology↗

bioRxiv2022

Progressive spread of chromosomal inversions blends the role of colonization and evolution in a parallel Galapagos beetle radiation

Archipelago island fauna include some of the most compelling examples of parallel adaptation to ecological gradients. However, despite the insuslar nature of these systems, the possibility that repeated instances of within-island divergence resulted from independent (in situ) evolutionary rather than repeated colonization events remains most often unclear. Here, we investigated the genomic underpinning of a progressive adaptive radiation of caterpillar-hunter beetles (Calosoma) in the low- and highland habitats from the Galapagos. These Calosoma beetles have evolved only partially reduced wings in the highland of the youngest islands but evolved to distinct short-winged species in the highland of the oldest islands. In support of independent evolutionary events, the extent of genome-wide divergence between long-winged lowland and short-winged highland populations decreased towards younger islands. However, in support of repeated colonization events, adaptation to highland habitats was driven by repeated selection of alleles that are shared across all highland species and populations. These alleles comprised extensive chromosomal inversions whose origin was traced back to an initial high-lowland divergence event on the oldest island. Moreover, we found evidence that after this initial divergence event, highland alleles spread to younger islands through dispersal of highland individuals as well as dispersal of lowland individuals that were polymorphic at adaptive loci, both providing the opportunity for the establishment of highland populations on the younger islands. These findings highlight the importance of an old divergence in driving repeated adaptation to ecological gradients. Complex histories of colonization and introgression may thus result in a mixed contribution of inter-island dispersal and within-island evolution in shaping parallel species communities on islands.

evolutionary biology↗

bioRxiv2022

A butterfly pan-genome reveals a large amount of structural variation underlies the evolution of chromatin accessibility

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 closely related Heliconius butterfly species. Over the relatively short evolutionary timescales investigated, up to 18.0% of the genome was composed of indels between two haplotypes of an individual H. charithonia butterfly and up to 62.7% included lineage-specific SVs between the genomes of the most distant species (11 Mya). Lineage-specific sequences were mostly characterized as transposable elements (TEs) inserted at random throughout the genome and their overall distribution was similarly affected by linked selection as single nucleotide substitutions. Using chromatin accessibility profiles (i.e., ATAC-seq) of head tissue in caterpillars to identify sequences with potential cis-regulatory function, we found that out of the 31,066 identified differences in chromatin accessibility between species, 30.4% were within lineage-specific SVs and 9.4% were characterized as TE insertions. These TE insertions were localized closer to gene transcription start sites than expected at random and were enriched for several transcription factor binding site candidates with known function in neuron development in Drosophila. We also identified 24 TE insertions with head-specific chromatin accessibility. Our results show high rates of structural genome evolution that were previously overlooked in comparative genomic studies and suggest a high potential for structural variation to serve as raw material for adaptive evolution.

genomics↗

bioRxiv2022

recolorize: improved color segmentation of digital images (for people with other things to do)

Color is an important source of biological information in fields ranging from disease ecology to sexual selection. Despite its importance, most metrics for color are restricted to point measurements. Methods for moving beyond point measurements rely on color maps, where every pixel in an image is assigned to one of a set of discrete color classes (color segmentation). Manual methods for color segmentation are slow and subjective, while existing automated methods often fail due to biological variation in pattern, technical variation in images, and poor scalability for batch clustering. As a result, color segmentation is the common bottleneck step for a majority of existing downstream analyses. Here we present recolorize, an R package for color segmentation that succeeds in many cases where existing methods fail. Recolorize has three major components: (1) an effective two-part clustering algorithm where color distributions are binned and combined according to perceived similarity in a frequency-independent manner; (2) a toolkit for minor manual adjustments to automatic output where needed; and (3) flexible export options. This paper illustrates how to use recolorize and compares it to existing methods, including examples where we segment formerly intractable images, and demonstrates the downstream use of methods that rely on color maps.

bioinformatics↗

bioRxiv2021

Evidence for a selective link between cooperation and individual recognition

The ability to recognize and discriminate among others is a frequent assumption of models of the evolution of cooperative behavior. At the same time, cooperative behavior has been proposed as a selective agent favoring the evolution of individual recognition abilities. While theory predicts that recognition and cooperation may co-evolve, data linking recognition abilities and cooperative behavior with fitness or evidence of selection are elusive. Here, we provide evidence of a fitness link between individual recognition and cooperation in the paper wasp Polistes fuscatus. Nest founding females in northern populations frequently form cooperative multiple foundress nests and possess highly variable facial patterns that mediate individual recognition. We describe a dearth of cooperative nesting, low phenotypic diversity, and a lack of individual recognition in southern populations. In a common garden experiment, northern co-foundress associations successfully reared offspring while all cooperative southern groups failed to rear any offspring, suggesting a fitness link between individual recognition and successful cooperation. Consistent with a selective link between individual recognition and cooperation, we find that rates of cooperative co-nesting correlate with identity-signaling color pattern diversity across the species range. Moreover, genomic evidence of recent positive selection on cognition loci likely to mediate individual recognition is substantially stronger in northern compared to southern P. fuscatus populations. Collectively, these data suggest that individual recognition and cooperative nesting behavior have co-evolved in P. fuscatus because recognition helps mediate conflict among co-nesting foundresses. This work provides evidence of a specific cognitive phenotype under selection because of social interactions, supporting the idea that social behavior can be a key driver of cognitive evolution.

animal behavior and cognition↗

bioRxiv2021

A masculinizing supergene underlies an exaggerated male reproductive morph in a spider.

In many species, individuals can develop into strikingly different morphs, which are determined by a simple Mendelian locus. How selection shapes loci that control complex phenotypic differences remains poorly understood. In the spider Oedothorax gibbosus, males either develop into a hunched morph with conspicuous head structures or as a fast developing flat morph with a female-like appearance. We show that the hunched-differs from the flat-determining allele by a hunch-specific genomic fragment of approximately 3 megabases. This fragment comprises dozens of genes that duplicated from genes found at different chromosomes. All functional duplicates, including doublesex - a key sexual differentiation regulatory gene, show male-specific expression, which illustrates their combined role as a masculinizing supergene. Our findings demonstrate how extensive indel polymorphisms and duplications of regulatory genes may contribute to the evolution of co-adapted gene clusters, sex-limited reproductive morphs, and the enigmatic evolution of exaggerated sexual traits in general.

evolutionary biology↗

bioRxiv2020

Selection and gene flow define polygenic barriers between incipient butterfly species

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 generate heterogenous genomic landscapes of divergence which make inferences about the regions that are responsible for species boundaries problematic. However, as the signal of admixture and selection on genomic loci varies with recombination rate, their relationship can be used to infer their relative importance during speciation. Here, we explore patterns of genomic divergence, admixture and recombination rate among hybridizing lineages across the Heliconius erato radiation. We focus on the incipient species, H. erato and H. himera, and distinguish the processes that drive genomic divergence across three contact zones where they frequently hybridize. Using demographic modeling and simulations, we infer that periods of isolation and selection have been major causes of genome-wide correlation patterns between recombination rate and divergence between these incipient species. Upon secondary contact, we found surprisingly highly asymmetrical introgression between the species pair, with a paucity of H. erato alleles introgressing into the H. himera genomes. We suggest that this signal may result from a current polygenic species boundary between the hybridizing lineages. These results contribute to a growing appreciation for the importance of polygenic architectures of species boundaries and pervasive genome-wide selection during the early stages of speciation with gene flow.

evolutionary biology↗

bioRxiv2020

The march of the Common Green Iguana (Iguana iguana): early establishment in Singapore and Thailand is facilitated by the pet trade and recreational parks

The popularity of the Common Green Iguana (Iguana iguana) as a pet has contributed to its global occurrence as an invasive alien species. Early detection and control of invasive alien I. iguana populations is necessary to prevent the need for large and financially demanding eradication actions. Here, we collated information from digital footage and interviews regarding sightings of free roaming I. iguana specimens in Singapore and Thailand, and present evidence of early-stage invasions and establishment. Using species distribution modeling, we find that large parts of Thailand and neighboring countries have suitable habitat, which could facilitate the expansion of these alien populations if left uncontrolled. Additionally, we report singular I. iguana sightings in Hong Kong and Peninsular Malaysia. We call for awareness of alien I. iguana in the Philippines due to the high number of pet iguanas and reported CITES importations as well as the availability of suitable habitat throughout the archipelago. Further, we identify I. iguana presence to be facilitated by the release of pet-traded specimens and uncontrolled exhibition practices in recreational parks. We provide recommendations for implementing monitoring and eradication efforts and strategy recommendations to halt future spread and release.

ecology↗

bioRxiv2020

Perfect mimicry between Heliconius butterflies is constrained by genetics and development

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 resemblance in melanic patterning across the mid-forewing that has been linked to expression patterns of the gene WntA. Recent CRISPR/Cas9 experiments have informed us on the exact areas of the wings in which WntA affects color pattern formation in both H. erato and H. melpomene, thus providing a unique comparative dataset to explore the functioning of a gene and its potential effect on phenotypic evolution. We therefore quantified wing color pattern differences in the mid-forewing region of 14 co-mimetic races of H. erato and H. melpomene and measured the extent to which mimicking races are not perfectly identical. While the relative size of the mid-forewing pattern is generally nearly identical, our results highlight the areas of the wing that prevent these species from achieving perfect mimicry and demonstrate that this mismatch can be largely explained by constraints imposed by divergence in the gene regulatory network that define wing color patterning. Divergence in the developmental architecture of a trait can thus constrain morphological evolution even between relatively closely related species.

evolutionary biology↗

bioRxiv2019

Classic and introgressed selective sweeps shape mimicry loci across a butterfly adaptive radiation

Natural selection leaves distinct signatures in the genome that can reveal the targets and history of adaptive evolution. By analysing high-coverage genome sequence data from four major colour pattern loci sampled from nearly 600 individuals in 53 populations, we show pervasive selection on wing patterns across the Heliconius adaptive radiation. The strongest signatures correspond to loci with the greatest phenotypic effects, consistent with visual selection by predators, and are found in colour patterns with geographically restricted distributions. These recent sweeps are similar between co-mimics and indicate colour pattern turn-over events despite strong stabilizing selection. Using simulations we compare sweep signatures expected under classic hard sweeps with those resulting from adaptive introgression, an important aspect of mimicry evolution in Heliconius. Simulated recipient populations show a distinct volcano pattern with peaks of increased genetic diversity around the selected target, consistent with patterns found in some populations. Our genomic data provide unprecedented insights into the recent history of selection across the Heliconius adaptive radiation.

evolutionary biology↗

bioRxiv2017

Patterns of Z chromosome divergence among Heliconius species highlight the importance of historical demography

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 sex chromosome compared to autosomes, such patterns could be interpreted as evidence for faster divergence on the sex chromosome, i.e. faster-X, or barriers to gene flow on the sex chromosome. However, demographic changes can strongly skew divergence estimates and are not always taken into consideration. We used 224 whole genome sequences representing 36 populations from two Heliconius butterfly clades (H. erato and H. melpomene) to explore patterns of Z chromosome divergence. We show that increased divergence compared to equilibrium expectations can in many cases be explained by demographic change. Among Heliconius erato populations, for instance, population size increase in the ancestral population can explain increased absolute divergence measures on the Z chromosome compared to the autosomes, as a result of increased ancestral Z chromosome genetic diversity. Nonetheless, we do identify increased divergence on the Z chromosome relative to the autosomes in parapatric or sympatric species comparisons that imply post-zygotic reproductive barriers. Using simulations, we show that this is consistent with reduced gene flow on the Z chromosome, perhaps due to greater accumulation of species incompatibilities. Our work demonstrates the importance of constructing an appropriate demographic null model in order to interpret patterns of divergence on the Z chromosome, but nonetheless provides evidence to support the Z chromosome as a strong barrier to gene flow in incipient Heliconius butterfly species.

evolutionary biology↗

bioRxiv2017

Patternize: An R Package For Quantifying Color Pattern Variation

O_LIThe 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 organisms.\nC_LIO_LIpatternize is an R package that quantifies variation in color patterns obtained from image data. patternize first defines homology between pattern positions across specimens either through manually placed homologous landmarks or automated image registration. Pattern identification is performed by categorizing the distribution of colors using an RGB threshold, k-means clustering or watershed transformation.\nC_LIO_LIWe demonstrate that patternize can be used for quantification of the color patterns in a variety of organisms by analyzing image data for butterflies, guppies, spiders and salamanders. Image data can be compared between sets of specimens, visualized as heatmaps and analyzed using principal component analysis (PCA).\nC_LIO_LIpatternize has potential applications for fine scale quantification of color pattern phenotypes in population comparisons, genetic association studies and investigating the basis of color pattern variation across a wide range of organisms.\nC_LI

bioinformatics↗