Drift and Directional Selection Are the Evolutionary Forces Driving Gene Expression Divergence in Eye and Brain Tissue of<i>Heliconius</i>Butterflies

Catalán, Ana; Briscoe, Adriana D.; Höhna, Sebastian

doi:10.1534/genetics.119.302493

Cited by 36 publications

(40 citation statements)

References 102 publications

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“…Moreover targeted RT-PCR on a subset of these genes suggested that selection could occur simultaneously in the coding sequence and regulatory elements of these genes. Overall our work, together with previous studies (Catalan, Höhna, et al. 2019; Catalan, Macias-Munoz, et al.…”

Section: Discussionsupporting

confidence: 76%

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Comparative Transcriptomics Provides Insights into Reticulate and Adaptive Evolution of a Butterfly Radiation

Zhang

León-Ricardo

Schooten

et al. 2019

Genome Biology and Evolution

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Butterfly eyes are complex organs that are composed of a diversity of proteins and they play a central role in visual signaling and ultimately, speciation, and adaptation. Here, we utilized the whole eye transcriptome to obtain a more holistic view of the evolution of the butterfly eye while accounting for speciation events that co-occur with ancient hybridization. We sequenced and assembled transcriptomes from adult female eyes of eight species representing all major clades of the Heliconius genus and an additional outgroup species, Dryas iulia. We identified 4,042 orthologous genes shared across all transcriptome data sets and constructed a transcriptome-wide phylogeny, which revealed topological discordance with the mitochondrial phylogenetic tree in the Heliconius pupal mating clade. We then estimated introgression among lineages using additional genome data and found evidence for ancient hybridization leading to the common ancestor of Heliconius hortense and Heliconius clysonymus. We estimated the Ka/Ks ratio for each orthologous cluster and performed further tests to demonstrate genes showing evidence of adaptive protein evolution. Furthermore, we characterized patterns of expression for a subset of these positively selected orthologs using qRT-PCR. Taken together, we identified candidate eye genes that show signatures of adaptive molecular evolution and provide evidence of their expression divergence between species, tissues, and sexes. Our results demonstrate: 1) greater evolutionary changes in younger Heliconius lineages, that is, more positively selected genes in the cydno–melpomene–hecale group as opposed to the sara–hortense–erato group, and 2) suggest an ancient hybridization leading to speciation among Heliconius pupal-mating species.

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Section: Discussionsupporting

confidence: 76%

“…2010). It is worth pointing out that while most of these studies on a specific group of visual genes have increased our understanding of color perception, only a few of them have addressed the adaptive evolutionary signature of an entire butterfly eye (Catalan, Höhna, et al. 2019; Catalan, Macias-Munoz, et al.…”

Section: Introductionmentioning

confidence: 99%

Comparative Transcriptomics Provides Insights into Reticulate and Adaptive Evolution of a Butterfly Radiation

Zhang

León-Ricardo

Schooten

et al. 2019

Genome Biology and Evolution

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“…Most of the main genes involved in D. melanogaster phototransduction were found as single copies in Lepidoptera and were upregulated in H. melpomene heads such as Gqα , β and γ , norpA , inaD , ninaC , Calx , trp , trpl , Arr1 , Arr2 , and stops (fig. 1; Table 2, for additional orthocluster analysis in butterflies see Catalán et al. 2018).…”

Section: Resultsmentioning

confidence: 99%

Evolution of Phototransduction Genes in Lepidoptera

Macias-Muñoz

Olguin

Briscoe

2019

Genome Biology and Evolution

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Vision is underpinned by phototransduction, a signaling cascade that converts light energy into an electrical signal. Among insects, phototransduction is best understood in Drosophila melanogaster. Comparison of D. melanogaster against three insect species found several phototransduction gene gains and losses, however, lepidopterans were not examined. Diurnal butterflies and nocturnal moths occupy different light environments and have distinct eye morphologies, which might impact the expression of their phototransduction genes. Here we investigated: 1) how phototransduction genes vary in gene gain or loss between D. melanogaster and Lepidoptera, and 2) variations in phototransduction genes between moths and butterflies. To test our prediction of phototransduction differences due to distinct visual ecologies, we used insect reference genomes, phylogenetics, and moth and butterfly head RNA-Seq and transcriptome data. As expected, most phototransduction genes were conserved between D. melanogaster and Lepidoptera, with some exceptions. Notably, we found two lepidopteran opsins lacking a D. melanogaster ortholog. Using antibodies we found that one of these opsins, a candidate retinochrome, which we refer to as unclassified opsin (UnRh), is expressed in the crystalline cone cells and the pigment cells of the butterfly, Heliconius melpomene. Our results also show that butterflies express similar amounts of trp and trpl channel mRNAs, whereas moths express ∼50× less trp, a potential adaptation to darkness. Our findings suggest that while many single-copy D. melanogaster phototransduction genes are conserved in lepidopterans, phototransduction gene expression differences exist between moths and butterflies that may be linked to their visual light environment.

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“…For both models roughly 99% of the prior MASV is greater than 0.01, while roughly 5% of the posterior MASV is greater than 0.01, further indicating that the models are producing effectively constant trajectories. Computing such a significance threshold to reject a constant rate model can be computed using Monte Carlo simulation [ 58 ]. The HSMRF and GMRF produce very similar average error and fold change, though the distributions of these metrics for the GMRF are more tightly focused around the target values (MAD of 0, FC of 1), and the GMRF has slightly tighter credible intervals.…”

Section: Resultsmentioning

confidence: 99%

Locally adaptive Bayesian birth-death model successfully detects slow and rapid rate shifts

et al. 2020

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Birth-death processes have given biologists a model-based framework to answer questions about changes in the birth and death rates of lineages in a phylogenetic tree. Therefore birth-death models are central to macroevolutionary as well as phylodynamic analyses. Early approaches to studying temporal variation in birth and death rates using birth-death models faced difficulties due to the restrictive choices of birth and death rate curves through time. Sufficiently flexible time-varying birth-death models are still lacking. We use a piecewise-constant birth-death model, combined with both Gaussian Markov random field (GMRF) and horseshoe Markov random field (HSMRF) prior distributions, to approximate arbitrary changes in birth rate through time. We implement these models in the widely used statistical phylogenetic software platform RevBayes, allowing us to jointly estimate birth-death process parameters, phylogeny, and nuisance parameters in a Bayesian framework. We test both GMRF-based and HSMRF-based models on a variety of simulated diversification scenarios, and then apply them to both a macroevolutionary and an epidemiological dataset. We find that both models are capable of inferring variable birth rates and correctly rejecting variable models in favor of effectively constant models. In general the HSMRF-based model has higher precision than its GMRF counterpart, with little to no loss of accuracy. Applied to a macroevolutionary dataset of the Australian gecko family Pygopodidae (where birth rates are interpretable as speciation rates), the GMRF-based model detects a slow decrease whereas the HSMRF-based model detects a rapid speciation-rate decrease in the last 12 million years. Applied to an infectious disease phylodynamic dataset of sequences from HIV subtype A in Russia and Ukraine (where birth rates are interpretable as the rate of accumulation of new infections), our models detect a strongly elevated rate of infection in the 1990s.

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Drift and Directional Selection Are the Evolutionary Forces Driving Gene Expression Divergence in Eye and Brain Tissue ofHeliconiusButterflies

Abstract: Characterization of gene expression patterns across species - and the evolutionary forces driving them - can reveal processes that have remained conserved across species, as well as those that have changed in a species- specific manner...

Cited by 36 publications

References 102 publications

Comparative Transcriptomics Provides Insights into Reticulate and Adaptive Evolution of a Butterfly Radiation

Comparative Transcriptomics Provides Insights into Reticulate and Adaptive Evolution of a Butterfly Radiation

Evolution of Phototransduction Genes in Lepidoptera

Locally adaptive Bayesian birth-death model successfully detects slow and rapid rate shifts

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