Phylogenomic Assessment of the Role of Hybridization and Introgression in Trait Evolution

Wang, Yaxuan; Cao, Zhen; Ogilvie, Huw A.; Nakhleh, Luay

doi:10.1101/2020.09.16.300343

Cited by 6 publications

(7 citation statements)

References 56 publications

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“…This may suggest that a sizeable fraction of the Anisozygoptera genome descends from zygopteran lineages. Taken together, these observations strongly suggest xenoplasious origin [93] of Anisozygopteran traits (i.e. traits introduced to a recipient taxon via introgression) that are shared with Zygoptera.…”

Section: Ancestral Introgression As An Evolutionary Driver In Anisozymentioning

confidence: 80%

Deep ancestral introgression shapes evolutionary history of dragonflies and damselflies

Suvorov

Scornavacca

Fujimoto

et al. 2020

Preprint

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exchange of inter-specific genetic information via various biological processes. In particular, 51 lateral gene transfer, incomplete lineage sorting (ILS) and introgression can result in gene trees 52 that are discordant with the species tree [3, 4]. Lateral transfer and introgression both involve 53 gene flow following speciation, thereby producing "reticulate" phylogenies. Incomplete lineage 54 sorting (ILS), on the other hand, occurs when three or more lineages coalesce in their ancestral 55 population. This often arises in an order that conflicts with that of the true species tree, and thus 56 involves no post-speciation gene flow and therefore does not contribute to reticulate evolution. 57 Thus, phylogenetic species-gene tree incongruence observed in empirical data can provide 58 insight into underlying biological factors that shape the evolutionary trajectories of a set of taxa. 59The major source of reticulate evolution for eukaryotes is introgression where it affects 60 approximately 25% of flowering plant and 10% of animal species [1, 5]. Introgressed alleles can 61 be fitness-neutral, deleterious [6] or adaptive. For example, adaptive introgression has been 62 shown to provide an evolutionary rescue from polluted habitats in gulf killifish (Fundulus 63 grandis) [7], yielded mimicry adaptations among Heliconius butterflies [8] and archaic 64 introgression has facilitated adaptive evolution of altitude tolerance [9], immunity and 65 metabolism in modern humans [10]. Additionally, hybridization and introgression are important 66 and often overlooked mechanisms of invasive species establishment and spread [11]. 67Odonata, the insect order that contains dragonflies and damselflies, lacks a strongly 68 supported backbone tree to clearly resolve higher-level phylogenetic relationships [12, 13]. 69 Current evidence places odonates together with Ephemeroptera (mayflies) as the living 70 representatives of the most ancient insect lineages to have evolved wings and active flight [14]. 71Odonates possess unique anatomical and morphological features such as a specialized body 72 form, specialized wing venation, a distinctive form of muscle attachment to the wing base [15] 73 allowing for direct flight and accessory (secondary) male genitalia that support certain unique 74 behaviors (e.g., sperm competition). They are among the most adept flyers of all animals and are 75 exclusively carnivorous insects relying primarily on vision [16, 17] to capture prey. They spend 76 much of their adult life in flight [18]. Biogeographically, odonates exhibit worldwide dispersal 77[19] and play crucial ecological roles in local freshwater communities, being a top invertebrate 78 predator [20]. Due to this combination of characteristics, odonates are quickly becoming model 79 organisms to study specific questions in ecology, physiology and evolution [21, 22]. However, 80 the extent of introgression at the genomic scale within Odonata remains primarily unknown. 81Two early attempts to tackle introgression/hybridization patterns wi...

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Section: Ancestral Introgression As An Evolutionary Driver In Anisozymentioning

confidence: 80%

Deep ancestral introgression shapes evolutionary history of dragonflies and damselflies

Suvorov

Scornavacca

Fujimoto

et al. 2020

Preprint

View full text Add to dashboard Cite

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“…To study the effects of introgression on the probability of hemiplasy, we combine concepts from two previously published models: the ‘parent tree’ framework of Hibbins and Hahn, 2019 , and the model of binary-trait evolution presented in Guerrero and Hahn, 2018 (see Wang et al, 2020 for an alternative way to extend the model to incorporate introgression). Consider a rooted three-taxon tree with the topology ((A,B), C).…”

Section: Resultsmentioning

confidence: 99%

Determining the probability of hemiplasy in the presence of incomplete lineage sorting and introgression

Hibbins

Gibson

Hahn

2020

eLife

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The incongruence of character states with phylogenetic relationships is often interpreted as evidence of convergent evolution. However, trait evolution along discordant gene trees can also generate these incongruences – a phenomenon known as hemiplasy. Classic comparative methods do not account for discordance, resulting in incorrect inferences about the number, timing, and direction of trait transitions. Biological sources of discordance include incomplete lineage sorting (ILS) and introgression, but only ILS has received theoretical consideration in the context of hemiplasy. Here, we present a model that shows introgression makes hemiplasy more likely, such that methods that account for ILS alone will be conservative. We also present a method and software (HeIST) for making statistical inferences about the probability of hemiplasy and homoplasy in large datasets that contain both ILS and introgression. We apply our methods to two empirical datasets, finding that hemiplasy is likely to contribute to the observed trait incongruences in both.

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“…The characters were traced on the phylogeny of the cpDNA data using ML method (Figs. 7, 8 and 9) because of the potential hemiplasy and xenoplasy produced by the discordance and hybridization detected in the nuclear backbone (Avies and Robinson 2008; Robinson et al, 2008; Copetti et al, 2017; Wang et al, 2020). A consequence of this discordance is elevated levels of apparent homoplasy in the species tree (Copetti et al, 2017; Hahn and Nakhleh 2017).…”

Section: Discussionmentioning

confidence: 99%

“…(e.g., Judd et al,1994; Donoghue et al, 2001; Stevens, 2001 onwards; Wang et al, 2015; Wang et al, 2020). To maximize stability and ease identification based on recent phylogenetic studies (e.g., Li et al, 2019; Wang et al, 2020; Xiang et al, 2020), we prefer the Caprifoliaceae s.l. concept that includes seven major clades: Linnaeoideae, Zabelia , Morinoideae, Valerianoideae, Dipsacoideae, Caprifolioideae and Diervilloideae (Stevens, 2001 onwards; Wang et al, 2015; APG, 2016; Wang et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

A phylogenomic perspective on gene tree conflict and character evolution in Caprifoliaceae using target enrichment data, with Zabelioideae recognized as a new subfamily

Wang

Morales‐Briones

Moore

et al. 2020

Preprint

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The use of diverse datasets in phylogenetic studies aiming for understanding evolutionary histories of species can yield conflicting inference. Phylogenetic conflicts observed in animal and plant systems have often been explained by hybridization, incomplete lineage sorting (ILS), or horizontal gene transfer. Here, we employed target enrichment data and species tree and species network approaches to infer the backbone phylogeny of the family Caprifoliaceae, while distinguishing among sources of incongruence. We used 713 nuclear loci and 46 protein-coding sequences of plastome data from 43 samples representing 38 species from all major clades to reconstruct the phylogeny of the group using concatenation and coalescence approaches. We found significant nuclear gene tree conflict as well as cytonuclear discordance. Additionally, coalescent simulations and phylogenetic species network analyses suggest putative ancient hybridization among subfamilies of Caprifoliaceae, which seems to be the main source of phylogenetic discordance. Ancestral state reconstruction of six morphological characters revealed some homoplasy for each character examined. By dating the branching events, we inferred the origin of Caprifoliaceae at approximately 69.38 Ma in the late Cretaceous. By integrating evidence from molecular phylogeny, divergence times, and morphology, we herein recognize Zabelioideae as a new subfamily in Caprifoliaceae. This work shows the necessity to use a combination of multiple approaches to identify the sources of gene tree discordance. Our study also highlights the importance of using data from both nuclear and chloroplast genomes to reconstruct deep and shallow phylogenies of plants.

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Phylogenomic Assessment of the Role of Hybridization and Introgression in Trait Evolution

Cited by 6 publications

References 56 publications

Deep ancestral introgression shapes evolutionary history of dragonflies and damselflies

Deep ancestral introgression shapes evolutionary history of dragonflies and damselflies

Determining the probability of hemiplasy in the presence of incomplete lineage sorting and introgression

A phylogenomic perspective on gene tree conflict and character evolution in Caprifoliaceae using target enrichment data, with Zabelioideae recognized as a new subfamily

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