Biology subjects

Darragh, K.

Publications and source records attributed to Darragh, K..

12 recordsLinked to original sources

bioRxiv2026

Evolutionary contingency facilitates scent divergence in an emergent orchid population

Reproductive isolation can evolve rapidly even among populations with extensive genetic similarity, but the mechanisms underlying this divergence remain an open question in evolutionary biology. Here, we investigate the genetic basis of floral scent divergence, a key trait mediating differential pollinator attraction, in a group of nascent Gongora orchid lineages that occur in sympatry. We combined whole-genome resequencing and floral transcriptomics to characterize the transition from the monoterpene-emitting 'M chemotype' to the pollinator-isolated phenylpropanoid-emitting 'A chemotype' nested within it. While overall genetic differentiation was low, a few highly differentiated regions contained candidate genes in biosynthetic pathways. Of particular interest was a putative o-methyltransferase exhibiting evidence of a recent selective sweep in the A chemotype, with much higher expression in scent-emitting floral tissues of A than in M. Transcriptomic comparison with a more distantly related monoterpene-emitting lineage ('X chemotype') further revealed the coordinated and elevated expression of phenylpropanoid biosynthetic genes in M despite its absence of aromatic floral volatiles, including a putative key enzyme potentially involved in directing metabolic flux towards monolignol biosynthesis. Together, our results support a model in which pre-existing activity in a metabolic pathway may facilitate the evolution of a novel floral scent phenotype, potentially making transitions across the adaptive landscape of scent more accessible than others. We propose that such evolutionary contingency may help explain how divergent scent profiles, and consequently, reproductive isolation, can evolve rapidly via few genetic changes.

evolutionary biology↗

bioRxiv2024

Repeated loss of floral scent in independent transitions from bee to hummingbird pollination in spiral gingers

The repeated evolution of the same trait in different lineages provides powerful natural experiments to study the phenotypic and genotypic predictability of how traits are gained and lost. A fascinating example of this is the repeated evolution of hummingbird pollination in plant lineages in the Americas, a widespread and often unidirectional phenomenon. The spiral gingers in the genus Costus are ancestrally bee-pollinated, and hummingbird pollination has evolved multiple times independently in the tropical Americas. These pollinator transitions are accompanied by predictable morphological and color changes, but the changes in floral scent have not been described. In this study, we describe the floral scent composition of 30 species of Costus sampled across the phylogeny to understand how floral scent has evolved across the genus with respect to pollinator transitions. We then combine transcriptomics and genomics to identify genetic expression differences and gene family evolution associated with pollinator transitions. We show that hummingbird-pollinated species have mostly lost their floral scent, whereas bee-pollinated species exhibit either floral scent maintenance or in some cases, gains of more diverse scent profiles. We find the floral scent loss appears to be due to gene downregulation rather than pseudogenization. The remarkable consistency of scent loss in hummingbird-pollinated species highlights the shared strong selection pressures experienced by these lineages. Even species with more recent transitions from bee to hummingbird pollination exhibit scent loss, highlighting the rapid breakdown of scent production following pollinator transitions. This research highlights the capacity for rapid changes when selection pressures are strong through downregulation of floral scent genes. ResumenLa evolucion independiente de un rasgo en diferentes linajes ofrece la oportunidad de estudiar la predictibilidad de fenotipos y sus bases geneticas. Un ejemplo fascinante es la evolucion repetida de polinizacion por colibries en varios linajes de plantas en las Americas, un fenomeno generalizado y tipicamente unidireccional. Las especies de cana agria del genero Costus son polinizadas ancestralmente por abejas y la polinizacion por colibries ha evolucionado varias veces de forma independiente en America tropical. Cada transicion de polinizador ha sido acompanada de varios cambios morfologicos y colores predecibles, pero los cambios en el aroma floral no han sido descritos. En este estudio describimos la composicion del aroma floral de 30 especies de Costus para comprender como el aroma floral ha evolucionado con respecto a las transiciones de polinizadores. Combinamos transcriptomica y genomica en un clado de Costus para identificar diferencias en la expresion genetica y la evolucion de la familia de genes asociadas con las transiciones de polinizadores. Nuestros resultados muestran que las especies polinizadas por colibries han perdido en su mayoria su aroma floral, mientras que las especies polinizadas por abejas ya sea mantienen el aroma floral y, en algunos casos, muestran ganancias de perfiles de aroma mas diversos. La consistencia en la perdida de olor en especies polinizadas por colibries resalta las fuertes presiones de seleccion natural que experimentan estos linajes. Incluso las especies con transiciones mas recientes de polinizacion de abejas a colibries exhiben perdida de olor, lo que destaca la rapida interrupcion de la produccion de olores despues de las transiciones de los polinizadores. Tambien encontramos que la perdida de aroma floral parece estar controlada por regulacion genica negativa y no por la perdida de genes de produccion de aromas (e.g. pseudogenizacion). Esta investigacion destaca la rapidez de cambios a traves de la regulacion negativa de genes que controlan aromas florales cuando las presiones de seleccion son fuertes. Significance StatementThe independent evolution of the same trait in different lineages provides a natural experiment to investigate the predictability of evolution. A fascinating example is the evolution of hummingbird pollination, which has occurred many times across flowering plants, and often involves convergence in multiple traits. In this study, we combine comparative chemical ecology with genomics and transcriptomics to study floral scent evolution in the genus Costus. We show that species exhibit loss of floral scent following transitions to hummingbird pollination suggesting a shared strong selection pressure favoring scent loss. We demonstrate the floral scent loss appears to be due to gene downregulation. This research highlights the capacity for rapid changes when selection pressures are strong through downregulation of scent genes.

evolutionary biology↗

bioRxiv2023

Adaptive divergence in the eyes of Heliconius butterflies likely contributes to pre- and post mating isolation

When populations experience different sensory conditions, natural selection may favor whole sensory system divergence, from the peripheral structures to the brain. We characterized the outer eye morphology of sympatric Heliconius species from different forest types, and their first-generation reciprocal hybrids to test for adaptive visual system divergence and hybrid disruption. In Panama, Heliconius cydno occurs in closed forests, whereas Heliconius melpomene resides in more open areas. Previous work has shown that, among wild individuals, H. cydno has larger eyes than H. melpomene, and there are heritable, habitat-associated differences in the visual brain structures that exceed neutral divergence expectations. Notably, hybrids have intermediate neural phenotypes, suggesting disruption. To test for similar effects in the visual periphery, we reared both species and their hybrids in common garden conditions. We confirm that H. cydno has larger eyes and provide new evidence that this is driven by selection. Hybrid eye morphology is more H. melpomene-like despite body size being intermediate, contrasting with neural trait intermediacy. Thus, eye morphology differences between H. cydno and H. melpomene are consistent with adaptive divergence, and when combined with previous neuroanatomy data, suggest hybrid visual system disruption due to mismatched patterns of intermediacy and dominance in the visual pathway.

evolutionary biology↗

bioRxiv2023

Individual variation in male pheromone production in carpenter bees correlates with size and sexual maturity.

Sex pheromones are species-specific chemical signals that facilitate the location, identification, and selection of mating partners. These pheromones can vary between individuals, and act as signals of mate quality. Here, we investigate the variation of male pheromones in the mesosomal glands of the large carpenter bee Xylocopa sonorina, within a Northern California population. We tested the hypothesis that morphological traits are correlated with the observed variation in chemical blend composition of these bees. We also conducted behavioral assays to test whether these male pheromones act as long-range attractants to conspecifics. We found that larger males with darker mesosomal glands have a higher pheromone amount in their glands. Our analysis also shows initial evidence that this pheromone blend serves as a long-range attractant to both males and females. We show that both male body size and sexual maturation are important factors influencing pheromone abundance, and that this pheromone blend acts as a long-range attractant. We hypothesize that this recorded variation in male pheromone could be important for female choice.

evolutionary biology↗

bioRxiv2022

Seasonal stability and species specificity of environmentally acquired chemical mating signals in orchid bees

Traits that mediate reproductive isolation between species, such as those involved in mate choice and/or recognition, are predicted to experience stabilizing selection towards the species mean. Male orchid bees collect chemical compounds from many sources, such as plants and fungi, which they use as a perfume signal (pheromone) during courtship display. Environmentally acquired signals are more prone to variation as source availability can vary through space and time. Here, we investigate the seasonality and species-specificity of male perfumes across an entire year in three sympatric species of Euglossa orchid bees. Our analysis revealed considerable within-species variation in perfumes. However, species-specificity was maintained consistently throughout the year, suggesting that these perfumes could play an important role in reproductive isolation. Our analysis also identified strong correlations in the abundance of some compounds, possibly due to shared collection sources between species. Our study suggests that orchid bee perfumes are robust in the face of environmental changes in resource availability.

evolutionary biology↗

bioRxiv2021

The birth-and-death evolution of cytochrome P450 genes in bees

The birth-and-death model of multigene family evolution describes how families can expand by duplication and contract by gene deletion and formation of pseudogenes. The phylogenetic stability of a gene is thought to be related to the degree of functional importance. However, it is unclear how much evolution of a gene in a gene family is driven by adaptive versus neutral processes. The cytochrome P450s are one of the most diverse and well-studied multigene families, involved in both physiological and xenobiotic functions. Bees have a high toxin exposure due to their diet of nectar and pollen, as well as the resin-collecting behavior exhibited by some bees. Here, we describe the P450s of the orchid bee Euglossa dilemma. Orchid bees are a neotropical clade in which males form perfume bouquets used in courtship displays by collecting a diverse set of volatile compounds, resulting in high chemical compound exposure. We conducted phylogenetic and selection analyses across ten bee species encompassing three bee families. We do not find a relationship between the ecology of a bee species and its P450 repertoire. Our analyses reveal that P450 clades can be classified into stable and unstable clades, and that genes involved in xenobiotic metabolism are more likely to belong to unstable clades. Furthermore, we find that unstable clades are under more dynamic evolutionary pressures, with signals of adaptive evolution detected, suggesting that both gene duplication and positive selection driving sequence divergence have played a role in the diversification of bee P450s. Our works highlights the complexity of multigene family evolution which does not always follow generalized predictions. Significance statementGene family evolution is characterized by deletion and duplication, but it is unclear if this is driven by adaptive or neutral evolutionary processes. To investigate the dynamics of gene family evolution we analyze the P450s of ten bee species, a well-studied gene family involved in both physiological and detoxification roles. We find that genes involved in detoxification are more likely to belong to unstable clades, exhibit dynamic evolutionary pressures, and show signals of adaptive evolution. However, we do not find evidence for a relationship between resin collection or sociality, and the P450 repertoire of a bee species. Our findings highlight the complexity of multigene family evolution which does not always follow generalized predictions.

molecular biology↗

bioRxiv2020

Clustering of loci controlling species differences in chemical bouquets of sympatric Heliconius butterflies

The degree to which loci promoting reproductive isolation cluster in the genome - i.e. the genetic architecture of reproductive isolation - can influence the tempo and mode of speciation. Tight linkage between these loci can facilitate speciation in the face of gene flow. Pheromones play a role in reproductive isolation in many Lepidoptera species, and the role of endogenously-produced compounds as secondary metabolites decreases the likelihood of pleiotropy associated with many barrier loci. Heliconius butterflies use male sex pheromones to both court females (aphrodisiac wing pheromones) and ward off male courtship (male-transferred anti-aphrodisiac genital pheromones), and it is likely that these compounds play a role in reproductive isolation between Heliconius species. Using a set of backcross hybrids between H. melpomene and H. cydno, we investigated the genetic architecture of putative male pheromone compound production. We found a set of 40 significant quantitative trait loci (QTL) representing 33 potential pheromone compounds. QTL clustered significantly on two chromosomes, chromosome 8 for genital compounds and chromosome 20 for wing compounds, and chromosome 20 was enriched for potential pheromone biosynthesis genes. There was minimal overlap between pheromone QTL and known QTL for mate choice and color pattern. Nonetheless, we did detect linkage between a QTL for wing androconial area and optix, a color pattern locus known to play a role in reproductive isolation in these species. This tight clustering of putative pheromone loci might contribute to coincident reproductive isolating barriers, facilitating speciation despite ongoing gene flow.

evolutionary biology↗

bioRxiv2019

Chemical signals act as the main reproductive barrier between sister and mimetic Heliconius butterflies

Colour pattern has been long recognised as the trait that drives mate recognition between Heliconius species that are phylogenetically close. However, when this cue is compromised such as in cases of mimetic, sympatric and closely related species, alternative mating signals must evolve to ensure reproductive isolation and species integrity. The closely related species Heliconius melpomene malleti and H. timareta florencia, occur in the same geographic region and despite being co-mimics they display strong reproductive isolation. In order to test which cues differ between species, and therefore potentially contribute to reproductive isolation, we quantified differences in wing phenotype and male chemical profile. As expected, wing colour pattern was indistinguishable between the two species while the chemical profile of their male sex pheromones showed marked differences. We then conducted behavioural experiments to study the importance of these signals in mate recognition by females. In agreement with our previous results, we found that pheromones and not wing colour pattern drive the preference of females by conspecific males. In addition, experiments with hybrid males and females suggested an important genetic component for both pheromone production and preference. Altogether, these results suggest that pheromones are the major reproductive barrier opposing gene flow between these two sister and co-mimic species.

evolutionary biology↗

bioRxiv2019

A novel terpene synthase produces an anti-aphrodisiac pheromone in the butterfly Heliconius melpomene

Terpenes, a group of structurally diverse compounds, are the biggest class of secondary metabolites. While the biosynthesis of terpenes by enzymes known as terpene synthases (TPSs) has been described in plants and microorganisms, few TPSs have been identified in insects, despite the presence of terpenes in multiple insect species. Indeed, in many insect species, it remains unclear whether terpenes are sequestered from plants or biosynthesised de novo. No homologs of plant TPSs have been found in insect genomes, though insect TPSs with an independent evolutionary origin have been found in Hemiptera and Coleoptera. In the butterfly Heliconius melpomene, the monoterpene (E)-{beta}-ocimene acts as an anti-aphrodisiac pheromone, where it is transferred during mating from males to females to avoid re-mating by deterring males. To date only one insect monoterpene synthase has been described, in Ips pini (Coleoptera), and is a multifunctional TPS and isoprenyl diphosphate synthase (IDS). Here, we combine linkage mapping and expression studies to identify candidate genes involved in the biosynthesis of (E)-{beta}-ocimene. We confirm that H. melpomene has two enzymes that exhibit TPS activity, and one of these, HMEL037106g1 is able to synthesise (E)-{beta}-ocimene in vitro. Unlike the enzyme in Ips pini, these enzymes only exhibit residual IDS activity, suggesting they are more specialised TPSs, akin to those found in plants. Phylogenetic analysis shows that these enzymes are unrelated to previously described plant and insect TPSs. The distinct evolutionary origin of TPSs in Lepidoptera suggests that they have evolved multiple times in insects.\n\nSignificance statementTerpenes are a diverse class of natural compounds, used by both plants and animals for a variety of functions, including chemical communication. In insects it is often unclear whether they are synthesised de novo or sequestered from plants. Some plants and insects have converged to use the same compounds. For instance, (E)-{beta}-ocimene is a common component of floral scent and is also used by the butterfly Heliconius melpomene as an anti-aphrodisiac pheromone. We describe two novel terpene synthases, one of which synthesises (E)-{beta}-ocimene in H. melpomene, unrelated not only to plant enzymes but also other recently identified insect terpene synthases. This provides the first evidence that the ability to synthesise terpenes has arisen multiple times independently within the insects.

biochemistry↗

bioRxiv2019

A major locus controls a biologically active pheromone component in Heliconius melpomene

Understanding the production, response, and genetics of signals used in mate choice can inform our understanding of the evolution of both intraspecific mate choice and reproductive isolation. Sex pheromones are important for courtship and mate choice in many insects, but we know relatively little of their role in butterflies. The butterfly Heliconius melpomene uses a complex blend of wing androconial compounds during courtship. Electroantennography in H. melpomene and its close relative H. cydno showed that responses to androconial extracts were not species-specific. Females of both species responded equally strongly to extracts of both species, suggesting conservation of peripheral nervous system elements across the two species. Individual blend components provoked little to no response, with the exception of octadecanal, a major component of the H. melpomene blend. Supplementing octadecanal on the wings of octadecanal-rich H. melpomene males led to an increase in the time until mating, demonstrating the bioactivity of octadecanal in Heliconius. Using quantitative trait locus (QTL) mapping, we identified a single locus on chromosome 20 responsible for 41% of the parental species difference in octadecanal production. This QTL does not overlap with any of the major wing color or mate choice loci, nor does it overlap with known regions of elevated or reduced FST. A set of 16 candidate fatty acid biosynthesis genes lies underneath the QTL. Pheromones in Heliconius carry information relevant for mate choice and are under simple genetic control, suggesting they could be important during speciation.

evolutionary biology↗

bioRxiv2019

Species specificity and intraspecific variation in the chemical profiles of Heliconius butterflies across a large geographic range

In many animals, mate choice is important for the maintenance of reproductive isolation between species. Traits important for mate choice and behavioural isolation are predicted to be under strong stabilising selection within species, however such traits can also exhibit variation at the population level driven by neutral and adaptive evolutionary processes. Here, we describe patterns of divergence among androconial and genital chemical profiles at inter- and intra-specific levels in mimetic Heliconius butterflies. Most variation in chemical bouquets was found between species, but there were also quantitative differences at the population level. We found a strong correlation between interspecific chemical and genetic divergence, however, this correlation varied in intraspecific comparisons. We identified indicator compounds characteristic of particular species that included known biologically active compounds, suggesting an approach for identification of candidate compounds for future behavioural studies in novel systems. Overall, the strong signal of species identity suggests a role for these compounds in species recognition, but with additional potentially neutral variation at the population level.

evolutionary biology↗

bioRxiv2018

Male pheromone composition depends on larval but not adult diet in Heliconius melpomene

Condition-dependent traits can act as honest signals of mate quality, with fitter individuals able to display preferred phenotypes. Nutrition is known to be an important determinant of individual condition, with diet known to affect many secondary sexual traits. In Heliconius butterflies, male chemical signalling plays an important role in female mate choice. Heliconius pheromones are sexually dimorphic, found only in mature males, but it is unclear what information they convey to the female. Here, we manipulate both the larval and adult diet of male Heliconius melpomene rosina to test for environmental effects on wing and genital pheromone production. We find no evidence that adult pollen consumption affects pheromone production in the first ten days after eclosion. We also find strong overlap in the chemical profiles of individuals reared on different larval host plants. However, individual compounds were found in different amounts between host plant treatments. Further electrophysiological and behavioural experiments will be needed to determine the biological significance of these differences.

ecology↗