De Novo Genes Arise at a Slow but Steady Rate along the Primate Lineage and Have Been Subject to Incomplete Lineage Sorting

ABSTRACTPhylogenetic analyses of trait evolution can provide insight into the evolutionary processes that initiate and drive phenotypic diversification. However, recent phylogenomic studies have revealed extensive gene tree-species tree discordance, which can lead to incorrect inferences of trait evolution if only a single species tree is used for analysis. This phenomenon—dubbed “hemiplasy”—is particularly important to consider during analyses of character evolution in rapidly radiating groups, where discordance is widespread. Here we generate whole-transcriptome data for a phylogenetic analysis of 14 species in the plant genus Jaltomata (the sister clade to Solanum), which has experienced rapid, recent trait evolution, including in fruit and nectar color, and flower size and shape. Consistent with other radiations, we find evidence for rampant gene tree discordance due to incomplete lineage sorting (ILS) and several introgression events among the well-supported subclades. Since both ILS and introgression increase the probability of hemiplasy, we perform several analyses that take discordance into account while identifying genes that might contribute to phenotypic evolution. Despite discordance, the history of fruit color evolution in Jaltomata can be inferred with high confidence, and we find evidence of de novo adaptive evolution at individual genes associated with fruit color variation. In contrast, hemiplasy appears to strongly affect inferences about floral character transitions in Jaltomata, and we identify candidate loci that could arise either from multiple lineage-specific substitutions or standing ancestral polymorphisms. Our analysis provides a generalizable example of how to manage discordance when identifying loci associated with trait evolution in a radiating lineage.

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Disentangling Population History and Character Evolution among Hybridizing Lineages

Molecular Biology and Evolution ◽

10.1093/molbev/msaa004 ◽

2020 ◽

Vol 37 (5) ◽

pp. 1295-1305 ◽

Cited By ~ 1

Author(s):

Sean P Mullen ◽

Nicholas W VanKuren ◽

Wei Zhang ◽

Sumitha Nallu ◽

Evan B Kristiansen ◽

...

Keyword(s):

Evolutionary Biology ◽

De Novo ◽

Balancing Selection ◽

Incomplete Lineage Sorting ◽

Introgressive Hybridization ◽

Character Evolution ◽

Population History ◽

Lineage Sorting ◽

Evolutionary Origins ◽

Whole Genome Resequencing

Abstract Understanding the origin and maintenance of adaptive phenotypic novelty is a central goal of evolutionary biology. However, both hybridization and incomplete lineage sorting can lead to genealogical discordance between the regions of the genome underlying adaptive traits and the remainder of the genome, decoupling inferences about character evolution from population history. Here, to disentangle these effects, we investigated the evolutionary origins and maintenance of Batesian mimicry between North American admiral butterflies (Limenitis arthemis) and their chemically defended model (Battus philenor) using a combination of de novo genome sequencing, whole-genome resequencing, and statistical introgression mapping. Our results suggest that balancing selection, arising from geographic variation in the presence or absence of the unpalatable model, has maintained two deeply divergent color patterning haplotypes that have been repeatedly sieved among distinct mimetic and nonmimetic lineages of Limenitis via introgressive hybridization.

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Plastomes of eight Ligusticum species: characterization, genome evolution, and phylogenetic relationships

BMC Plant Biology ◽

10.1186/s12870-020-02696-7 ◽

2020 ◽

Vol 20 (1) ◽

Author(s):

Ting Ren ◽

Zi-Xuan Li ◽

Deng-Feng Xie ◽

Ling-Jian Gui ◽

Chang Peng ◽

...

Keyword(s):

Phylogenetic Relationships ◽

De Novo ◽

Incomplete Lineage Sorting ◽

Phylogenetic Analyses ◽

Morphological Characteristics ◽

Purifying Selection ◽

Repeat Sequence ◽

Lineage Sorting ◽

Plastome Evolution ◽

Tree Topologies

Abstract Background The genus Ligusticum consists of approximately 60 species distributed in the Northern Hemisphere. It is one of the most taxonomically difficult taxa within Apiaceae, largely due to the varied morphological characteristics. To investigate the plastome evolution and phylogenetic relationships of Ligusticum, we determined the complete plastome sequences of eight Ligusticum species using a de novo assembly approach. Results Through a comprehensive comparative analysis, we found that the eight plastomes were similar in terms of repeat sequence, SSR, codon usage, and RNA editing site. However, compared with the other seven species, L. delavayi exhibited striking differences in genome size, gene number, IR/SC borders, and sequence identity. Most of the genes remained under the purifying selection, whereas four genes showed relaxed selection, namely ccsA, rpoA, ycf1, and ycf2. Non-monophyly of Ligusticum species was inferred from the plastomes and internal transcribed spacer (ITS) sequences phylogenetic analyses. Conclusion The plastome tree and ITS tree produced incongruent tree topologies, which may be attributed to the hybridization and incomplete lineage sorting. Our study highlighted the advantage of plastome with mass informative sites in resolving phylogenetic relationships. Moreover, combined with the previous studies, we considered that the current taxonomy system of Ligusticum needs to be improved and revised. In summary, our study provides new insights into the plastome evolution, phylogeny, and taxonomy of Ligusticum species.

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Large-scale ruminant genome sequencing provides insights into their evolution and distinct traits

Science ◽

10.1126/science.aav6202 ◽

2019 ◽

Vol 364 (6446) ◽

pp. eaav6202 ◽

Cited By ~ 54

Author(s):

Lei Chen ◽

Qiang Qiu ◽

Yu Jiang ◽

Kun Wang ◽

Zeshan Lin ◽

...

Keyword(s):

Large Scale ◽

De Novo ◽

Incomplete Lineage Sorting ◽

Regulatory Elements ◽

Habitat Diversity ◽

Human Populations ◽

Population Declines ◽

Lineage Sorting ◽

Ruminant Species ◽

System Metabolism

The ruminants are one of the most successful mammalian lineages, exhibiting morphological and habitat diversity and containing several key livestock species. To better understand their evolution, we generated and analyzed de novo assembled genomes of 44 ruminant species, representing all six Ruminantia families. We used these genomes to create a time-calibrated phylogeny to resolve topological controversies, overcoming the challenges of incomplete lineage sorting. Population dynamic analyses show that population declines commenced between 100,000 and 50,000 years ago, which is concomitant with expansion in human populations. We also reveal genes and regulatory elements that possibly contribute to the evolution of the digestive system, cranial appendages, immune system, metabolism, body size, cursorial locomotion, and dentition of the ruminants.

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Genomic architecture and introgression shape a butterfly radiation

Science ◽

10.1126/science.aaw2090 ◽

2019 ◽

Vol 366 (6465) ◽

pp. 594-599 ◽

Cited By ~ 64

Author(s):

Nathaniel B. Edelman ◽

Paul B. Frandsen ◽

Michael Miyagi ◽

Bernardo Clavijo ◽

John Davey ◽

...

Keyword(s):

Gene Flow ◽

Adaptive Radiation ◽

Phylogenetic Relationships ◽

De Novo ◽

Incomplete Lineage Sorting ◽

Color Pattern ◽

Lineage Sorting ◽

Genome Sequences ◽

Genomic Architecture ◽

Genome Assemblies

We used 20 de novo genome assemblies to probe the speciation history and architecture of gene flow in rapidly radiating Heliconius butterflies. Our tests to distinguish incomplete lineage sorting from introgression indicate that gene flow has obscured several ancient phylogenetic relationships in this group over large swathes of the genome. Introgressed loci are underrepresented in low-recombination and gene-rich regions, consistent with the purging of foreign alleles more tightly linked to incompatibility loci. Here, we identify a hitherto unknown inversion that traps a color pattern switch locus. We infer that this inversion was transferred between lineages by introgression and is convergent with a similar rearrangement in another part of the genus. These multiple de novo genome sequences enable improved understanding of the importance of introgression and selective processes in adaptive radiation.

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Faculty Opinions recommendation of Widespread discordance of gene trees with species tree in Drosophila: evidence for incomplete lineage sorting.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1052717.504629 ◽

2006 ◽

Author(s):

Artyom Kopp

Keyword(s):

Incomplete Lineage Sorting ◽

Species Tree ◽

Gene Trees ◽

Lineage Sorting

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The Perfect Storm: Gene Tree Estimation Error, Incomplete Lineage Sorting, and Ancient Gene Flow Explain the Most Recalcitrant Ancient Angiosperm Clade, Malpighiales

Systematic Biology ◽

10.1093/sysbio/syaa083 ◽

2020 ◽

Author(s):

Liming Cai ◽

Zhenxiang Xi ◽

Emily Moriarty Lemmon ◽

Alan R Lemmon ◽

Austin Mast ◽

...

Keyword(s):

Gene Flow ◽

Incomplete Lineage Sorting ◽

Estimation Error ◽

Gene Tree ◽

Species Tree ◽

Flowering Plant ◽

Estimation Methods ◽

Lineage Sorting ◽

Tree Estimation ◽

Perfect Storm

Abstract The genomic revolution offers renewed hope of resolving rapid radiations in the Tree of Life. The development of the multispecies coalescent (MSC) model and improved gene tree estimation methods can better accommodate gene tree heterogeneity caused by incomplete lineage sorting (ILS) and gene tree estimation error stemming from the short internal branches. However, the relative influence of these factors in species tree inference is not well understood. Using anchored hybrid enrichment, we generated a data set including 423 single-copy loci from 64 taxa representing 39 families to infer the species tree of the flowering plant order Malpighiales. This order includes nine of the top ten most unstable nodes in angiosperms, which have been hypothesized to arise from the rapid radiation during the Cretaceous. Here, we show that coalescent-based methods do not resolve the backbone of Malpighiales and concatenation methods yield inconsistent estimations, providing evidence that gene tree heterogeneity is high in this clade. Despite high levels of ILS and gene tree estimation error, our simulations demonstrate that these two factors alone are insufficient to explain the lack of resolution in this order. To explore this further, we examined triplet frequencies among empirical gene trees and discovered some of them deviated significantly from those attributed to ILS and estimation error, suggesting gene flow as an additional and previously unappreciated phenomenon promoting gene tree variation in Malpighiales. Finally, we applied a novel method to quantify the relative contribution of these three primary sources of gene tree heterogeneity and demonstrated that ILS, gene tree estimation error, and gene flow contributed to 10.0%, 34.8%, and 21.4% of the variation, respectively. Together, our results suggest that a perfect storm of factors likely influence this lack of resolution, and further indicate that recalcitrant phylogenetic relationships like the backbone of Malpighiales may be better represented as phylogenetic networks. Thus, reducing such groups solely to existing models that adhere strictly to bifurcating trees greatly oversimplifies reality, and obscures our ability to more clearly discern the process of evolution.

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Morphological, Ecological, and Molecular Divergence of Conogethes pinicolalis from C. punctiferalis (Lepidoptera: Crambidae)

Insects ◽

10.3390/insects12050455 ◽

2021 ◽

Vol 12 (5) ◽

pp. 455

Author(s):

Na Ra Jeong ◽

Min Jee Kim ◽

Sung-Soo Kim ◽

Sei-Woong Choi ◽

Iksoo Kim

Keyword(s):

Phylogenetic Analysis ◽

First Generation ◽

Incomplete Lineage Sorting ◽

Divergence Time ◽

Sequence Divergence ◽

Lineage Sorting ◽

Mitochondrial Coi ◽

Feeding Type ◽

Pine Trees ◽

Yellow Peach Moth

Conogethes pinicolalis has long been considered as a Pinaceae-feeding type of the yellow peach moth, C. punctiferalis, in Korea. In this study, the divergence of C. pinicolalis from the fruit-feeding moth C. punctiferalis was analyzed in terms of morphology, ecology, and genetics. C. pinicolalis differs from C. punctiferalis in several morphological features. Through field observation, we confirmed that pine trees are the host plants for the first generation of C. pinicolalis larvae, in contrast to fruit-feeding C. punctiferalis larvae. We successfully reared C. pinicolalis larvae to adults by providing them pine needles as a diet. From a genetic perspective, the sequences of mitochondrial COI of these two species substantially diverged by an average of 5.46%; moreover, phylogenetic analysis clearly assigned each species to an independent clade. On the other hand, nuclear EF1α showed a lower sequence divergence (2.10%) than COI. Overall, EF1α-based phylogenetic analysis confirmed each species as an independent clade, but a few haplotypes of EF1α indicated incomplete lineage sorting between these two species. In conclusion, our results demonstrate that C. pinicolalis is an independent species according to general taxonomic criteria; however, analysis of the EF1α sequence revealed a short divergence time.

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Phylogenomic Discordance in the Eared Seals is best explained by Incomplete Lineage Sorting following Explosive Radiation in the Southern Hemisphere

Systematic Biology ◽

10.1093/sysbio/syaa099 ◽

2020 ◽

Author(s):

Fernando Lopes ◽

Larissa R Oliveira ◽

Amanda Kessler ◽

Yago Beux ◽

Enrique Crespo ◽

...

Keyword(s):

Incomplete Lineage Sorting ◽

Gene Tree ◽

Molecular Data ◽

Species Tree ◽

Gene Trees ◽

Lineage Sorting ◽

Data Types ◽

High Coverage ◽

Sea Lions ◽

The Family

Abstract The phylogeny and systematics of fur seals and sea lions (Otariidae) have long been studied with diverse data types, including an increasing amount of molecular data. However, only a few phylogenetic relationships have reached acceptance because of strong gene-tree species tree discordance. Divergence times estimates in the group also vary largely between studies. These uncertainties impeded the understanding of the biogeographical history of the group, such as when and how trans-equatorial dispersal and subsequent speciation events occurred. Here we used high-coverage genome-wide sequencing for 14 of the 15 species of Otariidae to elucidate the phylogeny of the family and its bearing on the taxonomy and biogeographical history. Despite extreme topological discordance among gene trees, we found a fully supported species tree that agrees with the few well-accepted relationships and establishes monophyly of the genus Arctocephalus. Our data support a relatively recent trans-hemispheric dispersal at the base of a southern clade, which rapidly diversified into six major lineages between 3 to 2.5 Ma. Otaria diverged first, followed by Phocarctos and then four major lineages within Arctocephalus. However, we found Zalophus to be non-monophyletic, with California (Z. californianus) and Steller sea lions (Eumetopias jubatus) grouping closer than the Galapagos sea lion (Z. wollebaeki) with evidence for introgression between the two genera. Overall, the high degree of genealogical discordance was best explained by incomplete lineage sorting resulting from quasi-simultaneous speciation within the southern clade with introgresssion playing a subordinate role in explaining the incongruence among and within prior phylogenetic studies of the family.

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