Evolutionary dynamics of genome size and content during the adaptive radiation of Heliconiini butterflies

Cicconardi, Francesco; Milanetti, Edoardo; Castro, Érika Cristina Pinheiro de; Mazo‐Vargas, Anyi; Belleghem, Steven M. Van; Ruggieri, Angelo; Rastas, Pasi; Hanly, Joseph J.; Evans, Elizabeth; Jiggins, Chris D.; McMillan, W. Owen; Papa, Riccardo; Marino, Daniele Di; Martin, Arnaud; Montgomery, Stephen H.

doi:10.1101/2022.08.12.503723

Cited by 10 publications

(20 citation statements)

References 163 publications

(155 reference statements)

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“…A similar distinction between the autosome-majority trees and the Z-chromosome tree was also found by Zhang et al (2016). All four scenarios a-d confirm paraphyly of the silvaniform species (H. besckei, H. numata and the pardalinus-hecale clade), consistent with some recent phylogenomic studies (Zhang et al 2016;Massardo et al 2020;Cicconardi et al 2023). Monophyly of the silvaniforms was suggested in concatenation/sliding-window analysis (Heliconius Genome Consortium 2012; Kozak et al 2015;Kozak et al 2021;Zhang et al 2021), but this conclusion may suffer from a failure to account for deep coalescence (Edwards et al 2016).…”

Section: Major Introgression Patterns In the Melpomene-silvaniform Cladesupporting

confidence: 86%

“…We next focus more closely on the melpomene-silvaniform clade (including H. besckei, H. numata and H. melpomene, represented by "BNM" in Figure 1A), one of the most phylogenetically difficult groups of Heliconius due to ongoing hybridization and extensive gene flow involving most members of the group (Mallet et al 2007). Previous studies have inferred conflicting introgression scenarios in this clade (Martin et al 2013;Zhang et al 2016;Jay et al 2018;Edelman et al 2019;Cicconardi et al 2023). We compiled a multilocus dataset from high-quality genome data comprising 8 (out of 15) species representing all major lineages within the clade: H. melpomene, H.…”

Section: Major Introgression Patterns In the Melpomene-silvaniform Cladementioning

confidence: 99%

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Major patterns in the introgression history ofHeliconiusbutterflies

Thawornwattana

Seixas

Yang

et al. 2023

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Gene flow between species is an important evolutionary process that can facilitate adaptation and lead to species diversification. It also makes reconstruction of species relationships difficult. Here, we use the full-likelihood multispecies coalescent (MSC) approach to estimate species phylogeny and major introgression events inHeliconiusbutterflies from whole-genome sequence data. We obtain a robust estimate of species branching order among major clades in the genus, including the "melpomene-silvaniform" group, which shows extensive historical and on-going gene flow. We obtain chromosome-level estimates of key parameters in the species phylogeny, including species divergence times, present-day and ancestral population sizes as well as the direction, timing, and intensity of gene flow. Our analysis leads to a phylogeny with introgression events that differ from those obtained in previous studies. We find that H. aoede most likely represents the earliest- branching lineage of the genus and that "silvaniform" species are paraphyletic within the melpomene-silvaniform group. Our phylogeny provides new, parsimonious histories for the origins of key traits in Heliconius, including pollen feeding and an inversion involved in wing pattern mimicry. Our results demonstrate the power and feasibility of the full-likelihood MSC approach for estimating species phylogeny and key population parameters despite extensive gene flow. The methods used here should be useful for analysis of other difficult species groups with high rates of introgression.

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Section: Major Introgression Patterns In the Melpomene-silvaniform Cladesupporting

confidence: 86%

Section: Major Introgression Patterns In the Melpomene-silvaniform Cladementioning

confidence: 99%

Major patterns in the introgression history ofHeliconiusbutterflies

Thawornwattana

Seixas

Yang

et al. 2023

Preprint

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“…All phylogenetic comparative analyses were conducted using a new phylogenetic tree of the Heliconiini generated from newly assembled genomes (6). To assemble additional genomes of Heliconius erato cyrbia , H. melpomene rosina , H. m. amaryllis , and H. cydno galanthus , short-read illumina data was downloaded from NCBI (National Centre for Biotechnology Information) and a reference-guided assembly approach adapted and extended from Lischer and Shimizu (7) adopted.…”

Section: Supplementary Materialsmentioning

confidence: 99%

Rapid expansion and visual specialization of learning and memory centers in Heliconiini butterflies

Couto

Young

Atzeni

et al. 2022

Preprint

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How do neural systems evolve to support new behaviors? Changes in the abundance and diversity of neural cell types, and their connectivity, shape brain composition and provide the substrate for behavioral variation. We describe a striking example of neural elaboration in an ecologically diverse tribe of Heliconiini butterflies. By building extensive new datasets of neural traits across the tribe, we identify major bursts in the size and cellular composition of the mushroom bodies, central brain structures essential for learning and memory. These expansion events are associated with increased innervation form visual centers and coincide with enhanced performance in multiple cognitive assays. This suite of neural and cognitive changes is likely tied to the emergence of derived foraging behaviors, facilitated by localized specialization of neural networks.

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“…As already discussed, access to pollen would become crucial at later stages of adulthood, but the remaining question is: where did the valine and isoleucine used for CG biosynthesis come from during the first weeks of Heliconius adulthood in the control group (sugar only)? A recent comparative genomic study has found that two hexamerins, storage proteins, have been duplicated multiple times in heliconiines (Cicconardi et al, 2022). Hexamerins might provide valine and isoleucine for CG biosynthesis during the beginning of their adulthood, if pollen is not available.…”

Section: Discussionmentioning

confidence: 99%

“…Cocoonases are used by moths for cocoon digestion during eclosion and moths contain only a single copy of this enzyme, while Heliconius have multiple copies (Harpel et al 2015; Smith et al 2018). Nonetheless, comparative genomics has shown that they are duplicated in all heliconiines, even those that do not pollen feed (Cicconardi et al, 2022).…”

Section: Introductionmentioning

confidence: 99%

Pollen-feeding delays reproductive senescence and maintains toxicity ofHeliconius erato

Castro

McPherson

Julian

et al. 2023

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Dietary shifts may act to ease energetic constraints and allow organisms to optimise life-history traits. Heliconius butterflies differ from other nectar-feeders due to their unique ability to digest pollen, which provides a reliable source of amino acids to adults. Pollen-feeding has been associated with prolonged adult lifespan and increased fertility, yet there is a lack of empirical data demonstrating how pollen consumption influences key fitness traits, including chemical defences and adult body weight, as well as fertility over the long lifespan. Here, we investigate the effect of pollen-feeding on fertility, weight and chemical defences, as well as offspring defences, controlling for butterfly age and sex. Recently emerged Heliconius erato butterflies of similar size were fed for 14 or 45 days on one of three diets: sugar solution only, or sugar solution replenished with either supplement or pollen. At the end of the experiment, oviposition assays were performed to evaluate fertility, and afterwards all butterflies and eggs were weighed and used for target metabolomics to quantify cyanogenic glucosides (CG). We found that there is an age-specific and sex-specific effect of pollen-feeding on butterfly weight, with both the sugar-only and amino-acid supplement diets reducing the weight of old females (45d), but not young females (14d) or males of any age. Females fed only sugar significantly reduce their egg-laying through adulthood, whereas females that have access to pollen maintain their fertility. Diet had a significant effect on the maintenance of the chemical defence of females, but not males. Curiously, even though females that have access to pollen are heavier, more toxic and lay more eggs, this does not translate into improvements in offspring defences, as eggs from butterflies of all ages and diet treatment had similar CG content. Our results emphasise the importance of controlling for age-specific and sex-specific effects in studies of life-history evolution and demonstrate that dietary novelty can relax energetic constraints.

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Evolutionary dynamics of genome size and content during the adaptive radiation of Heliconiini butterflies

Cited by 10 publications

References 163 publications

Major patterns in the introgression history ofHeliconiusbutterflies

Major patterns in the introgression history ofHeliconiusbutterflies

Rapid expansion and visual specialization of learning and memory centers in Heliconiini butterflies

Pollen-feeding delays reproductive senescence and maintains toxicity ofHeliconius erato

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