2020Systematic BiologyOpen access

The Multilocus Multispecies Coalescent: A Flexible New Model of Gene Family Evolution

Qiuyi Li, Céline Scornavacca, Nicolas Galtier, Yao-ban Chan

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Abstract

Incomplete lineage sorting (ILS), the interaction between coalescence and speciation, can generate incongruence between gene trees and species trees, as can gene duplication (D), transfer (T), and loss (L). These processes are usually modeled independently, but in reality, ILS can affect gene copy number polymorphism, that is, interfere with DTL. This has been previously recognized, but not treated in a satisfactory way, mainly because DTL events are naturally modeled forward-in-time, while ILS is naturally modeled backward-in-time with the coalescent. Here, we consider the joint action of ILS and DTL on the gene tree/species tree problem in all its complexity. In particular, we show that the interaction between ILS and duplications/transfers (without losses) can result in patterns usually interpreted as resulting from gene loss, and that the realized rate of D, T, and L becomes nonhomogeneous in time when ILS is taken into account. We introduce algorithmic solutions to these problems. Our new model, the multilocus multispecies coalescent, which also accounts for any level of linkage between loci, generalizes the multispecies coalescent (MSC) model and offers a versatile, powerful framework for proper simulation, and inference of gene family evolution. [Gene duplication; gene loss; horizontal gene transfer; incomplete lineage sorting; multispecies coalescent; hemiplasy; recombination.].

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Incomplete lineage sorting (ILS), the interaction between coalescence and speciation, can generate incongruence between gene trees and species trees, as can gene duplication (D), transfer (T), and loss (L). These processes are usually modeled independently, but in reality, ILS can affect gene copy number polymorphism, that is, interfere with DTL. This has been previously recognized, but not treated in a satisfactory way, mainly because DTL events are naturally modeled forward-in-time, while ILS is naturally modeled backward-in-time with the coalescent. Here, we consider the joint action of ILS and DTL on the gene tree/species tree problem in all its complexity. In particular, we show that the interaction between ILS and duplications/transfers (without losses) can result in patterns usually interpreted as resulting from gene loss, and that the realized rate of D, T, and L becomes nonhomogeneous in time when ILS is taken into account. We introduce algorithmic solutions to these problems. Our new model, the multilocus multispecies coalescent, which also accounts for any level of linkage between loci, generalizes the multispecies coalescent (MSC) model and offers a versatile, powerful framework for proper simulation, and inference of gene family evolution. [Gene duplication; gene loss; horizontal gene transfer; incomplete lineage sorting; multispecies coalescent; hemiplasy; recombination.].

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Available abstract

Incomplete lineage sorting (ILS), the interaction between coalescence and speciation, can generate incongruence between gene trees and species trees, as can gene duplication (D), transfer (T), and loss (L). These processes are usually modeled independently, but in reality, ILS can affect gene copy number polymorphism, that is, interfere with DTL. This has been previously recognized, but not treated in a satisfactory way, mainly because DTL events are naturally modeled forward-in-time, while ILS is naturally modeled backward-in-time with the coalescent. Here, we consider the joint action of ILS and DTL on the gene tree/species tree problem in all its complexity. In particular, we show that the interaction between ILS and duplications/transfers (without losses) can result in patterns usually interpreted as resulting from gene loss, and that the realized rate of D, T, and L becomes nonhomogeneous in time when ILS is taken into account. We introduce algorithmic solutions to these problems. Our new model, the multilocus multispecies coalescent, which also accounts for any level of linkage between loci, generalizes the multispecies coalescent (MSC) model and offers a versatile, powerful framework for proper simulation, and inference of gene family evolution. [Gene duplication; gene loss; horizontal gene transfer; incomplete lineage sorting; multispecies coalescent; hemiplasy; recombination.].

Key concepts: Coalescent theory, Biology, Gene duplication, Coalescence (physics), Gene, Lineage (genetic), Horizontal gene transfer, Tree (set theory)

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