Publication Search Results

ID: 157996
Type: article
Authors: Avila-Cervantes, Jose; Arias, Carlos; Venegas-Anaya, Miryam; Vargas, Marta; Larsson, Hans C. E.; McMillan, W. Owen
Abstract: The final formation of the Central American Isthmus (CAI) about 3.5 million years ago altered global ocean circulation, connected North and South America terrestrial biotas, and established the Caribbean Sea. The nature of this event creates a natural scenario to test vicariance, divergence, and speciation by allopatry. Studies have shown the effect of the CAI on marine and terrestrial species, but none have examined a large-bodied amphibious taxon. We used RAD sequencing on populations of the American crocodile (Crocodylus acutus) to study the genomic variation of C. acutus on both sides of the CAI, infer its demographic history, and measure the effect of the opening of the Panama Canal. Our results showed three genomic clusters: (1) Caribbean and the Panama Canal, (2) Pacific coast, and (3) Coiba island. The estimated divergence times between the Caribbean and Pacific populations are about 20,000 years ago, which is younger than the formation of the CAI, coinciding with the Last Glacial Maximum. We hypothesize the glacial/interglacial cycles facilitated gene flow between the Caribbean and Pacific crocodile populations after the formation of the CAI, masking any genomic divergence the CAI may have caused. There is no evidence of gene flow associated with the opening of the Panama Canal.

ID: 158773
Type: article
Authors: Bennett, Kelly L.; McMillan, W. Owen; Loaiza, Jose R.
Abstract: Local adaptation is important when predicting arthropod-borne disease risk because of its impacts on vector population fitness and persistence. However, the extent that vector populations are adapted to the environment generally remains unknown. Despite low population structure and high gene flow in Aedes aegypti mosquitoes across Panama, excepting the province of Bocas del Toro, we identified 128 candidate SNPs, clustered within 17 genes, which show a strong genomic signal of local environmental adaptation. This putatively adaptive variation occurred across fine geographical scales with the composition and frequency of candidate adaptive loci differing between populations in wet tropical environments along the Caribbean coast and dry tropical conditions typical of the Pacific coast. Temperature and vegetation were important predictors of adaptive genomic variation in Ae. aegypti with several potential areas of local adaptation identified. Our study lays the foundations of future work to understand whether environmental adaptation in Ae. aegypti impacts the arboviral disease landscape and whether this could either aid or hinder efforts of population control.

ID: 157931
Type: article
Authors: Byers, Kelsey J. R. P.; Darragh, Kathy; Fernanda Garza, Sylvia; Abondano Almeida, Diana; Warren, Ian A.; Rastas, Pasi M. A.; Merrill, Richard M.; Schulz, Stefan; McMillan, W. Owen; Jiggins, Chris D.
Abstract: The degree to which loci promoting reproductive isolation cluster in the genome-that is, 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 antiaphrodisiac 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.

ID: 159406
Type: article
Authors: Darragh, Kathy; Orteu, Anna; Black, Daniella; Byers, Kelsey J. R. P.; Szczerbowski, Daiane; Warren, Ian A.; Rastas, Pasi; Pinharanda, Ana; Davey, John W.; Fernanda Garza, Sylvia; Abondano Almeida, Diana; Merrill, Richard M.; McMillan, W. Owen; Schulz, Stefan; Jiggins, Chris D.
Abstract: Plants and insects often use the same compounds for chemical communication, but not much is known about the genetics of convergent evolution of chemical signals. The terpene (E)-beta-ocimene is a common component of floral scent and is also used by the butterfly Heliconius melpomene as an anti-aphrodisiac pheromone. While the biosynthesis of terpenes has been described in plants and microorganisms, few terpene synthases (TPSs) have been identified in insects. Here, we study the recent divergence of 2 species, H. melpomene and Heliconius cydno, which differ in the presence of (E)-beta-ocimene; combining linkage mapping, gene expression, and functional analyses, we identify 2 novel TPSs. Furthermore, we demonstrate that one, HmelOS, is able to synthesise (E)-beta-ocimene in vitro. We find no evidence for TPS activity in HcydOS (HmelOS ortholog of H. cydno), suggesting that the loss of (E)-beta-ocimene in this species is the result of coding, not regulatory, differences. The TPS enzymes we discovered are unrelated to previously described plant and insect TPSs, demonstrating that chemical convergence has independent evolutionary origins.

ID: 159196
Type: article
Authors: de Castro, Erika C. P.; Musgrove, Jamie; Bak, Soren; McMillan, W. Owen; Jiggins, Chris D.
Abstract: Host plant specialization is a major force driving ecological niche partitioning and diversification in insect herbivores. The cyanogenic defences of Passiflora plants keep most herbivores at bay, but not the larvae of Heliconius butterflies, which can both sequester and biosynthesize cyanogenic compounds. Here, we demonstrate that both Heliconius cydno chioneus and H. melpomene rosina have remarkable plasticity in their chemical defences. When feeding on Passiflora species with cyanogenic compounds that they can readily sequester, both species downregulate the biosynthesis of these compounds. By contrast, when fed on Passiflora plants that do not contain cyanogenic glucosides that can be sequestered, both species increase biosynthesis. This biochemical plasticity comes at a fitness cost for the more specialist H. m. rosina, as adult size and weight for this species negatively correlate with biosynthesis levels, but not for the more generalist H. c. chioneus. By contrast, H. m rosina has increased performance when sequestration is possible on its specialized host plant. In summary, phenotypic plasticity in biochemical responses to different host plants offers these butterflies the ability to widen their range of potential hosts within the Passiflora genus, while maintaining their chemical defences.

ID: 159541
Type: article
Authors: Kozak, Krzysztof M.; Joron, Mathieu; McMillan, W. O.; Jiggins, Chris D.
Abstract: How frequent is gene flow between species? The pattern of evolution is typically portrayed as a phylogenetic tree, yet gene flow between good species may be an important mechanism in diversification, spreading adaptive traits and leading to a complex pattern of phylogenetic incongruence. This process has thus far been studied mainly among a few closely related species, or in geographically restricted areas such as islands, but not on the scale of a continental radiation. Using a nearly complete genomic representation of 47 species in the genus, we demonstrate that admixture has played a role throughout the evolution of the charismatic Neotropical butterflies Heliconius. Modeling of phylogenetic networks based on the exome uncovers up to 13 instances of interspecific gene flow. Admixture is detected among the relatives of H. erato, as well as between the ancient lineages leading to modern clades. Interspecific gene flow played a role throughout the evolution of the genus, although the process has been most frequent in the clade of H. melpomene and relatives. We identify H. hecalesia and relatives as putative hybrids, including new evidence for introgression at the loci controlling the mimetic wing patterns. Models accounting for interspecific gene flow yield a more complete picture of the radiation as a network, which will improve our ability to study trait evolution in a realistic comparative framework.

ID: 158621
Type: article
Authors: Montgomery, Stephen H.; Rossi, Matteo; McMillan, W. Owen; Merrill, Richard M.
Abstract: The importance of behavioral evolution during speciation is well established, but we know little about how this is manifest in sensory and neural systems. A handful of studies have linked specific neural changes to divergence in host or mate preferences associated with speciation. However, the degree to which brains are adapted to local environmental conditions, and whether this contributes to reproductive isolation between close relatives that have diverged in ecology, remains unknown. Here, we examine divergence in brain morphology and neural gene expression between closely related, but ecologically distinct, Heliconius butterflies. Despite ongoing gene flow, sympatric species pairs within the melpomene-cydno complex are consistently separated across a gradient of open to closed forest and decreasing light intensity. By generating quantitative neuroanatomical data for 107 butterflies, we show that Heliconius melpomene and Heliconius cydno clades have substantial shifts in brain morphology across their geographic range, with divergent structures clustered in the visual system. These neuroanatomical differences are mirrored by extensive divergence in neural gene expression. Differences in both neural morphology and gene expression are heritable, exceed expected rates of neutral divergence, and result in intermediate traits in first-generation hybrid offspring. Strong evidence of divergent selection implies local adaptation to distinct selective optima in each parental microhabitat, suggesting the intermediate traits of hybrids are poorly matched to either condition. Neural traits may therefore contribute to coincident barriers to gene flow, thereby helping to facilitate speciation.

ID: 159745
Type: article
Authors: Van Belleghem, Steven M.; Cole, Jared M.; Montejo-Kovacevich, Gabriela; Bacquet, Caroline N.; McMillan, W. Owen; Papa, Riccardo; Counterman, Brian A.
Abstract: 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 divergence to reconstruct recent speciation in the erato clade of Heliconius butterflies. We focus on the genomic landscape of divergence across three contact zones of the species H. erato and H. himera. We show that these hybridizing species have an intermediate level of divergence in the erato clade, which fits with their incomplete levels of reproductive isolation. Using demographic modeling and the relationship between admixture and divergence with recombination rate variation, we reconstruct histories of gene flow, selection, and demographic change that explain the observed patterns of genomic divergence. We find that periods of isolation and selection within populations, followed by secondary contact with asymmetrical gene flow are key factors in shaping the heterogeneous genomic landscapes. Collectively, these results highlight the effectiveness of demographic modeling and recombination rate estimates to disentangling the distinct contributions of gene flow and selection to patterns of genomic divergence.

ID: 154060
Type: article
Authors: Byers, Kelsey J. R. P.; Darragh, Kathy; Musgrove, Jamie; Almeida, Diana Abondano; Garza, Sylvia Fernanda; Warren, Ian A.; Rastas, Pasi M.; Kučka, Marek; Chan, Yingguang Frank; Merrill, Richard M.; Schulz, Stefan; McMillan, W. O.; Jiggins, Chris D.
Abstract: 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. This article is protected by copyright. All rights reserved.

ID: 156593
Type: article
Authors: Cox, Christian L.; Alexander, Sean; Casement, Brianna; Chung, Albert K.; Curlis, John David; Degon, Zachariah; Dubois, Madeline; Falvey, Cleo; Graham, Zackary A.; Folfas, Edita; Gallegos Koyner, Maria A.; Neel, Lauren K.; Nicholson, Daniel J.; Perez, Dylan J. Padilla; Ortiz-Ross, Xochitl; Rosso, Adam A.; Taylor, Quinn; Thurman, Timothy J.; Williams, Claire E.; McMillan, W. O.; Logan, Michael L.

ID: 156598
Type: article
Authors: Darragh, Kathy; Montejo‐Kovacevich, Gabriela; Kozak, Krzysztof M.; Morrison, Colin R.; Figueiredo, Clarisse M. E.; Ready, Jonathan S.; Salazar, Camilo; Linares, Mauricio; Byers, Kelsey J. R. P.; Merrill, Richard M.; McMillan, W. O.; Schulz, Stefan; Jiggins, Chris D.

ID: 155777
Type: article
Authors: González-Rojas, M. F.; Darragh, K.; Robles, J.; Linares, M.; Schulz, S.; McMillan, W. O.; Jiggins, C. D.; Pardo-Diaz, C.; Salazar, C.
Abstract: Colour pattern is the main 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 geographical region, and despite being co-mimics, they display strong reproductive isolation. In order to test which cues differ between species, and potentially contribute to reproductive isolation, we quantified differences in the wing phenotype and the male chemical profile. As expected, the wing colour pattern was indistinguishable between the two species, while the chemical profile of the androconial and genital males' extracts 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 chemical blends and not wing colour pattern drive the preference of females for conspecific males. Also, experiments with hybrid males and females suggested an important genetic component for both chemical production and preference. Altogether, these results suggest that chemicals are the major reproductive barrier opposing gene flow between these two sister and co-mimic species.

ID: 156756
Type: article
Authors: Kapheim, Karen M.; Jones, Beryl M.; Pan, Hailin; Li, Cai; Harpur, Brock A.; Kent, Clement F.; Zayed, Amro; Ioannidis, Panagiotis; Waterhouse, Robert M.; Kingwell, Callum; Stolle, Eckart; Avalos, Arián; Zhang, Guojie; McMillan, W. O.; Wcislo, William T.
Abstract: Developmental plasticity generates phenotypic variation, but how it contributes to evolutionary change is unclear. Phenotypes of individuals in caste-based (eusocial) societies are particularly sensitive to developmental processes, and the evolutionary origins of eusociality may be rooted in developmental plasticity of ancestral forms. We used an integrative genomics approach to evaluate the relationships among developmental plasticity, molecular evolution, and social behavior in a bee species ( Megalopta genalis ) that expresses flexible sociality, and thus provides a window into the factors that may have been important at the evolutionary origins of eusociality. We find that differences in social behavior are derived from genes that also regulate sex differentiation and metamorphosis. Positive selection on social traits is influenced by the function of these genes in development. We further identify evidence that social polyphenisms may become encoded in the genome via genetic changes in regulatory regions, specifically in transcription factor binding sites. Taken together, our results provide evidence that developmental plasticity provides the substrate for evolutionary novelty and shapes the selective landscape for molecular evolution in a major evolutionary innovation: Eusociality.

ID: 155402
Type: article
Authors: Nguyen, Bryan N.; Shen, Elaine W.; Seemann, Janina; Correa, Adrienne M. S.; O'Donnell, James L.; Altieri, Andrew H.; Knowlton, Nancy; Crandall, Keith A.; Egan, Scott P.; McMillan, W. Owen; Leray, Matthieu
Abstract: Accurate, rapid, and comprehensive biodiversity assessments are critical for investigating ecological processes and supporting conservation efforts. Environmental DNA (eDNA) surveys show promise as a way to effectively characterize fine-scale patterns of community composition. We tested whether a single PCR survey of eDNA in seawater using a broad metazoan primer could identify differences in community composition between five adjacent habitats at 19 sites across a tropical Caribbean bay in Panama. We paired this effort with visual fish surveys to compare methods for a conspicuous taxonomic group. eDNA revealed a tremendous diversity of animals (8,586 operational taxonomic units), including many small taxa that would be undetected in traditional in situ surveys. Fish comprised only 0.07% of the taxa detected by a broad COI primer, yet included 43 species not observed in the visual survey. eDNA revealed significant differences in fish and invertebrate community composition across adjacent habitats and areas of the bay driven in part by taxa known to be habitat-specialists or tolerant to wave action. Our results demonstrate the ability of broad eDNA surveys to identify biodiversity patterns in the ocean. © 2020, The Author(s).

ID: 154845
Type: article
Authors: Pierotti, Michele E. R.; Wandycz, Anna; Wandycz, Pawel; Rebelein, Anja; Corredor, Vitor H.; Tashiro, Juliana H.; Castillo, Armando; Wcislo, William T.; McMillan, W. O.; Loew, Ellis R.
Abstract: Since all forms of mimicry are based on perceptual deception, the sensory ecology of the intended receiver is of paramount importance to test the necessary precondition for mimicry to occur, i.e. model-mimic misidentification, and to gain insight in the origin and evolutionary trajectory of the signals. Here we test the potential for aggressive mimicry by a group of coral reef fishes, the color polymorphic Hypoplectrus hamlets, from the point of view of their most common prey, small epibenthic gobies and mysid shrimp. We build visual models based on the visual pigments and spatial resolution of the prey, the underwater light spectrum and color reflectances of putative models and their hamlet mimics. Our results are consistent with one mimic-model relationship between the butter hamlet H. unicolor and its model the butterflyfish Chaetodon capistratus but do not support a second proposed mimic-model pair between the black hamlet H. nigricans and the dusky damselfish Stegastes adustus. We discuss our results in the context of color morphs divergence in the Hypoplectrus species radiation and suggest that aggressive mimicry in H. unicolor might have originated in the context of protective (Batesian) mimicry by the hamlet from its fish predators.

ID: 157397
Type: article
Authors: Pierotti, Michele E. R.; Wandycz, Anna; Wandycz, Pawel; Rebelein, Anja; Corredor, Vitor H.; Tashiro, Juliana H.; Castillo, Armando; Wcislo, William T.; McMillan, W. Owen; Loew, Ellis R.
Abstract: Since all forms of mimicry are based on perceptual deception, the sensory ecology of the intended receiver is of paramount importance to test the necessary precondition for mimicry to occur, that is, model-mimic misidentification, and to gain insight in the origin and evolutionary trajectory of the signals. Here we test the potential for aggressive mimicry by a group of coral reef fishes, the color polymorphic Hypoplectrus hamlets, from the point of view of their most common prey, small epibenthic gobies and mysid shrimp. We build visual models based on the visual pigments and spatial resolution of the prey, the underwater light spectrum and color reflectances of putative models and their hamlet mimics. Our results are consistent with one mimic-model relationship between the butter hamlet H. unicolor and its model the butterflyfish Chaetodon capistratus but do not support a second proposed mimic-model pair between the black hamlet H. nigricans and the dusky damselfish Stegastes adustus. We discuss our results in the context of color morphs divergence in the Hypoplectrus species radiation and suggest that aggressive mimicry in H. unicolor might have originated in the context of protective (Batesian) mimicry by the hamlet from its fish predators rather than aggressive mimicry driven by its prey.

ID: 157077
Type: article
Authors: Rossi, Matteo; Hausmann, Alexander E.; Thurman, Timothy J.; Montgomery, Stephen H.; Papa, Riccardo; Jiggins, Chris D.; McMillan, W. Owen; Merrill, Richard M.
Abstract: Abstract 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 conspecifics. Here, we couple QTL for divergence in visual preference behaviours with population genomic and gene expression analyses of neural tissue (central brain, optic lobes and ommatidia) across development in two sympatric Heliconius species. Within a region containing 200 genes, we identify five genes that are strongly associated with divergent visual preferences. Three of these have previously been implicated in key components of neural signalling (specifically an ionotropic glutamate receptor and two regucalcins ), and overall our candidates suggest shifts in behaviour involve changes in visual integration or processing. This would allow preference evolution without altering perception of the wider environment.

ID: 158187
Type: article
Authors: Rosso, Adam A.; Nicholson, Daniel J.; Logan, Michael L.; Chung, Albert K.; Curlis, John David; Degon, Zachariah M.; Knell, Robert J.; Garner, Trenton W. J.; McMillan, W. Owen; Cox, Christian L.
Abstract: Given that sexual signals are often expressed more highly in one sex than the other, they can impose a sex-specific cost of reproduction through parasitism. The two primary paradigms regarding the relationship of parasites to sexual signals are the good genes hypothesis and the immunocompetence handicap hypothesis; however, there are other ecological, morphological and energetic factors that might influence parasite infections in a sex-specific fashion. We tested the relationship between expression of a sexual signal (the dewlap) and ecological, morphological and energetic factors mediating ectoparasite (mite) load between male and female Panamanian slender anoles (Anolis apletophallus). We found that males were more highly parasitized than females because of the preponderance of ectoparasites on the larger dewlap of males. Indeed, ectoparasite infection increased with both body size and dewlap size in males but not in females, and parasite infection was related to energy storage in a sex-specific fashion for the fat bodies, liver and gonads. Our work and previous work on testosterone in anoles suggests that this pattern did not arise solely from immunosuppression by testosterone, but that mites prefer the dewlap as an attachment site. Thus, the expression of this sexual signal could incur a fitness cost that might structure life-history trade-offs.

ID: 157076
Type: article
Authors: Toure, M. Wyatt; Young, Fletcher J.; McMillan, W. Owen; Montgomery, Stephen H.
Abstract: For many pollinators, flowers provide predictable temporal schedules of resource availability, meaning an ability to learn time-dependent information could be widely beneficial. However, this ability has only been demonstrated in a handful of species. Observations of Heliconius butterflies suggest that they may have an ability to form time-dependent foraging preferences. Heliconius are unique among butterflies in actively collecting pollen, a dietary behaviour linked to spatio-temporally faithful 'trap-line' foraging. Time dependency of foraging preferences is hypothesized to allow Heliconius to exploit temporal predictability in alternative pollen resources. Here, we provide the first experimental evidence in support of this hypothesis, demonstrating that Heliconius hecale can learn opposing colour preferences in two time periods. This shift in preference is robust to the order of presentation, suggesting that preference is tied to the time of day and not due to ordinal or interval learning. However, this ability is not limited to Heliconius , as previously hypothesized, but also present in a related genus of non-pollen feeding butterflies. This demonstrates time learning likely pre-dates the origin of pollen feeding and may be prevalent across butterflies with less specialized foraging behaviours.

ID: 156403
Type: article
Authors: Van Schooten, Bas; Meléndez-Rosa, Jesyka; Van Belleghem, Steven M.; Jiggins, Chris D.; Tan, John D.; McMillan, W. O.; Papa, Riccardo