Phylogenomic analyses in Phrymaceae reveal extensive gene tree discordance in relationships among major clades

Abstract

Premise: Phylogenomic datasets using genomes and transcriptomes provide rich opportunities beyond resolving bifurcating phylogenetic relationships. Monkeyflower (Phrymaceae) is a model system for evolutionary ecology. However, it lacks a wellsupported phylogeny as a basis for a stable taxonomy and for macroevolutionary comparisons. Methods: We sampled 24 genomes and transcriptomes in Phrymaceae and closely related families, including eight newly sequenced transcriptomes. We reconstructed the phylogeny using IQ-TREE and ASTRAL, evaluated gene tree discordance using PhyParts, Quartet Sampling, and a cloudogram, and carried out reticulation analyses using PhyloNet and HyDe. We searched for whole genome duplication (WGD) events using chromosome numbers, synonymous distances, and gene duplication events as evidence. Results: Most gene trees support the monophyly of Phrymaceae and each of its tribes. Most gene trees also support tribe Mimuleae being sister to Phrymeae + Diplaceae + Leucocarpeae, with extensive gene tree discordance among the latter three. Despite the discordance, the monophyly of Mimulus s.l. is rejected, and no individual reticulation event among the Phrymaceae tribes is well-supported. Reticulation likely occurred among Erythranthe bicolor and closely related species. No ancient WGD was detected in Phrymaceae. Instead, small-scale duplications are among potential drivers of macroevolutionary diversification of Phrymaceae. Conclusions: We show that analysis of reticulate evolution is sensitive to taxon sampling and methods used. We also demonstrate that phylogenomic datasets using genomes and transcriptomes present rich opportunities to investigate gene family evolution and genome duplication events involved in lineage diversification and adaptation.

Transposition, duplication, and divergence of the telomerase RNA underlies the evolution ofMimulustelomeres

“…The section Simiolus and Erythranthe are phylogenetic sisters while Diplacus is the third outgroup (Beardsley and Olmstead 2002) and the three sections last shared a common ancestor 32-50 million years ago (Kumar et al 2017). Recent phylogenetic analyses indicate polyphyly of the genus Mimulus (Morales Briones et al 2022), and taxonomic revision has split these focal species into separate genera, Diplacus and Erythranthe (Barker et al 2012). However, following other recent work in the Phrymaceae, we have elected to retain the use of the name Mimulus for its historic significance and recognizability (see Lowry et al 2019).…”

Genomic incongruence accompanies the evolution of flower symmetry in Eudicots: a case study in the poppy family (Papaveraceae, Ranunculales)

“…(2023) infer a much later Cretaceous divergence time. We posit that the amount of (geological) time that elapsed since the Jurassic divergence we estimate from their MRCA, coupled with rapid, non-bifurcating diversification events (e.g., reticulation following polyploidy and hybridization; Morales-Briones et al., 2018 , 2021 , 2022 ) might have resulted in incomplete lineage sorting (ILS) in the nuclear compartment and might have obscured the order of relationships in the plastome, e.g., through plastid capture following hybrid speciation ( Folk et al., 2016 ; Liu et al, 2020 ; Yang et al, 2021b ). We argue that Eupteleaceae, which is part of the Arcto-Tertiary relict flora endemic to East Asia ( Cao et al., 2016 ), is indeed sister to all other ranunculalean families.…”

“…Although the two main biological sources of nuclear-plastid conflict, i.e. hybridization and ILS, have genomic signatures that are often difficult to discriminate ( Steenwyk et al., 2023 ; Stull et al, 2023 ), it is sometimes possible to differentiate between them ( Morales-Briones et al., 2018 , 2021 , 2022 ; Cai et al, 2021 ; Meleshko et al, 2021 ; McLay et al, 2023 ). In the case of Papaveraceae, it is possible to rule out allopolyploid hybridization as a potential cause of genomic discordances at nodes corresponding to floral symmetry transitions.…”

The Boechera model system for evolutionary ecology

“…Recent studies have clarified relationships within several different clades, including the Boechera fendleri group (Alexander et al, 2015b), the Boechera suffrutescens group (Morin et al, 2018), and the Boechera puberula group (Schilling et al, 2018). Similar issues—backbone discordance and hybridization—have complicated phylogenetic resolution of other, similarly diverse ecological model systems such as Mimulus (Beardsley et al, 2004; Morales‐Briones et al, 2022) and Aquilegia (Fior et al, 2013) Two additional issues lend further complexity to phylogenetic resolution of Boechera : (1) the prevalence of polyploids (Schranz et al, 2005) and (2) the possibility of de novo evolution of sexual populations from rare recombination in facultatively asexual lineages (Carman et al, 2019), which would result in novel hybrid species like those found in other plant groups (e.g., Rieseberg et al, 2003). Newer methods have enabled robust resolution of Brassicaceae more broadly (Nikolov et al, 2019).…”