Overcoming paralogy and incomplete lineage sorting to detect a phylogeographic signal: a GapC study of Armeria pungens

Botany ◽  
2009 ◽  
Vol 87 (2) ◽  
pp. 164-177 ◽  
Author(s):  
Rosalía Piñeiro ◽  
Andrea Costa ◽  
Javier Fuertes Aguilar ◽  
Gonzalo Nieto Feliner

Low-copy nuclear genes have been suggested as a promising source of independent phylogeographic markers in plants. However, the available studies at the intraspecific level have revealed that extracting information from them is frequently hampered by paralogy and lack of coalescence of alleles. It is thus relevant to test their utility with plants for which solid data from other markers are available. The aims of this study are to retrieve phylogeographic useful information in a low-copy nuclear gene by examining the congruence of the genetic variation with the geography, as well as with previous nuclear ribosomal, plastid, and amplified fragment length polymorphism (AFLP) markers. Seven combinations of primers have been assayed to characterize the structure of GapC (cytosolic glyceraldehyde 3-phosphate dehydrogenase) in Armeria pungens (Link) Hoffmanns. & Link, a linearly distributed Atlantic–Mediterranean disjunct sand-dune species. A matrix of 101 direct sequences from 71 individuals was analysed with statistical parsimony. To check the reliability of direct sequencing, 216 cloned sequences were also generated. Tests of recombination have also been attempted. By comparing nucleotide and amino acid sequences, three different paralogs (1, 2, 3) were identified of which paralog 2 was sampled for phylogeographic inference. Within this paralog, 13 alleles belonging in three different sequence types (I, II, III) were detected. These types are shown to correspond with lineages from the same locus whose splitting predates the origin of A. pungens, although type III could be a recent paralog. Allelic variation within types I and II followed a clear geographic trend supporting the two main genetic lineages detected in A. pungens with previous markers. This study suggests that information on the population history of a species can be retrieved, even if some uncertainty remains on the source of variation of low-copy nuclear gene sequences, either alleles from the same locus or paralogs.

2020 ◽  
Vol 37 (5) ◽  
pp. 1295-1305 ◽  
Author(s):  
Sean P Mullen ◽  
Nicholas W VanKuren ◽  
Wei Zhang ◽  
Sumitha Nallu ◽  
Evan B Kristiansen ◽  
...  

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.


2003 ◽  
Vol 17 (6) ◽  
pp. 711 ◽  
Author(s):  
Jason E. Bond ◽  
David A. Beamer ◽  
Marshal C. Hedin ◽  
Petra Sierwald

Jamaican millipedes in the Anadenobolus species complex provide an unusual case study of arthropods having undergone speciation in the absence of conspicuous divergence of male genitalia. Using landmark-based morphometrics, we examined shape deformation of the male anterior copulatory device in three genetically divergent yet morphologically cryptic species. A multivariate analysis of variance and relative warp analysis of nonuniform components show that although male genitalic shape is statistically different among species, many specimens are 'misplaced' in morphological space, perhaps consistent with a condition analogous to incomplete lineage sorting. A simulation of neutral nuclear gene coalescence suggests that such incomplete sorting is expected, given the depth of mtDNA divergences observed across species. The pronounced contrast between deep molecular v. incomplete genitalic divergence is at odds with the paradigm of selection-driven rapid change in male copulatory structure during arthropod speciation. Alternatively, we suggest that male genitalic divergence is evolving neutrally or in concert with other components of the genome (pleiotropy). Although we recognise the empirical validity of rapid genitalic divergence via sexual selection or sexual conflict, such models must be empirically tested using multiple lines of evidence. Accepting the rapid and divergent hypothesis without such multiple evidence scrutiny may result in a gross underestimation of evolutionary diversity and, subsequently, the misinterpretation of processes shaping genitalic change.


2020 ◽  
Author(s):  
Rebecca S. Taylor ◽  
Ashley C. Bramwell ◽  
Rute Clemente-Carvalho ◽  
Nicholas A. Cairns ◽  
Frances Bonier ◽  
...  

ABSTRACTThe golden-crowned (Zonotrichia atricapilla) and white-crowned (Z. leucophrys) sparrows have been presented as a compelling case for rapid speciation. They display divergence in song and plumage with overlap in their breeding ranges implying reproductive isolation, but have almost identical mitochondrial genomes. Previous research proposed hybridization and subsequent mitochondrial introgression as an alternate explanation, but lacked robust nuclear gene trees to distinguish between introgression and incomplete lineage sorting. We test for signatures of these processes between Z. atricapilla and Z. leucophrys, and investigate the relationships among Z. leucophrys subspecies, using mitochondrial sequencing and a reduced representation nuclear genomic dataset. Contrary to the paraphyly evident in mitochondrial gene trees, we confirmed the reciprocal monophyly of Z. atricapilla and Z. leucophrys using large panels of single nucleotide polymorphism (SNPs). The pattern of cytonuclear discordance is consistent with limited, historical hybridization and mitochondrial introgression, rather than a recent origin and incomplete lineage sorting between recent sister species. We found evidence of nuclear phylogeographic structure within Z. leucophrys with two distinct clades. Altogether, our results support the true species status of Z. atricapilla and Z. leucophrys, and indicate deeper divergences between the two species than inferred using mitochondrial markers. Our results demonstrate the limitations of relying solely on mitochondrial DNA for taxonomy, and raise questions about the possibility of selection on the mitochondrial genome during temperature oscillations (e.g. during the Pleistocene). Historical mitochondrial introgression facilitated by past environmental changes could cause erroneous dating of lineage splitting in other taxa when based on mitochondrial DNA alone.


2016 ◽  
Author(s):  
Karolina Węcek ◽  
Stefanie Hartmann ◽  
Johanna L. A. Paijmans ◽  
Ulrike Taron ◽  
Georgios Xenikoudakis ◽  
...  

AbstractRetracing complex population processes that precede extreme bottlenecks may be impossible using data from living individuals. The wisent (Bison bonasus), Europe’s largest terrestrial mammal, exemplifies such a population history, having gone extinct in the wild but subsequently restored by captive breeding efforts. Using low coverage genomic data from modern and historical individuals, we investigate population processes occurring before and after this extinction. Analysis of aligned genomes supports the division of wisent into two previously recognised subspecies, but almost half of the genomic alignment contradicts this population history as a result of incomplete lineage sorting and admixture. Admixture between subspecies populations occurred prior to extinction and subsequently during the captive breeding program. Admixture with the Bos cattle lineage is also widespread but results from ancient events rather than recent hybridisation with domestics. Our study demonstrates the huge potential of historical genomes for both studying evolutionary histories and for guiding conservation strategies.


2020 ◽  
Vol 89 (4) ◽  
pp. 353-372
Author(s):  
José A. Jurado-Rivera ◽  
Francesco Zapelloni ◽  
Joan Pons ◽  
Carlos Juan ◽  
Damià Jaume

The Hyalella species diversity in the high-altitude water bodies of the Andean Altiplano is addressed using mitochondrial cox1 sequences and implementing different molecular species delimitation criteria. We have recorded the presence of five major genetic lineages in the Altiplano, of which one seems to be exclusive to Lake Titicaca and nearby areas, whereas the rest occur also in other regions of South America. Eleven out of 36 South American entities diagnosed by molecular delimitation criteria in our study are likely endemic to the Titicaca and neighbouring water bodies. We have detected a remarkable disagreement between morphology and genetic data in the Titicacan Hyalella, with occurrence of several cases of the same morpho-species corresponding to several Molecular Operational Taxonomic Units (MOTUs), some even distantly related, and other instances where a particular MOTU is shared by a morphologically heterogeneous array of species, including species with body smooth and others with body heavily armoured. Species diversification and incongruence between morphological and molecular boundaries within this species assemblage may be associated to the sharp changes in hydrological conditions experienced by the water bodies of the Altiplano in the past, which included dramatic fluctuations in water level and salinity of Lake Titicaca. Such environmental shifts could have triggered rapid morphological changes and ecological differentiation within the Hyalella assemblage, followed by phenotypic convergence among the diverse lineages. Factors such as phenotypic plasticity, incomplete lineage sorting or admixture between divergent lineages might lie also at the root of the morphological-genetic incongruence described herein.


Author(s):  
Kevin Karbstein ◽  
Salvatore Tomasello ◽  
Ladislav Hodac ◽  
Franz G. Dunkel ◽  
Mareike Daubert ◽  
...  

AbstractSpecies are the basic units of biodiversity and evolution. Nowadays, they are widely considered as ancestor-descendant lineages. Their definition remains a persistent challenge for taxonomists due to lineage evolutionary role and circumscription, i.e., persistence in time and space, ecological niche or a shared phenotype of a lineage. Recognizing and delimiting species is particularly methodically challenging in fast-evolving, evolutionary young species complexes often characterized by low genetic divergence, hybrid origin, introgression and incomplete lineage sorting (ILS). Ranunculus auricomus is a large Eurasian apomictic polyploid complex that probably has arisen from the hybridization of a few sexual progenitor species. However, even delimitation and relationships of diploid sexual progenitors have been unclearly ranging from two to twelve species. Here, we present an innovative workflow combining phylogenomic methods based on 86,782 parameter-optimized RADseq loci and target enrichment of 663 nuclear genes together with geometric morphometrics to delimit sexual species in this evolutionary young complex (< 1 Mya). For the first time, we revealed a fully resolved and well-supported maximum likelihood (ML) tree phylogeny congruent to neighbor-net network and STRUCTURE results based on RADseq data. In a few clades, we found evidence of discordant patterns indicated by quartet sampling (QS) and reticulation events in the neighbor-net network probably caused by introgression and ILS. Together with coalescent-based species delimitation approaches based on target enrichment data, we found five main genetic lineages, with an allopatric distribution in Central and Southern Europe. A concatenated geometric morphometric data set including basal and stem leaves, as well as receptacles, revealed the same five main clusters. We accept those five morphologically differentiated, geographically isolated, genetic main lineages as species: R. cassubicifolius s.l. (incl. R. carpaticola), R. flabellifolius, R. envalirensis s.l. (incl. R. cebennensis), R. marsicus and R. notabilis s.l. (incl. R. austroslovenicus, R. calapius, R. mediocompositus, R. peracris and R. subcarniolicus). Our comprehensive workflow combing phylogenomic methods supported by geometric morphometrics proved to be successful in delimiting closely related sexual taxa and applying an evolutionary species concept, which is also transferable to other evolutionarily young species complexes.


Genetics ◽  
1991 ◽  
Vol 128 (2) ◽  
pp. 269-279
Author(s):  
W K Thomas ◽  
A C Wilson

Abstract Through direct sequencing methods, the mitochondrial gene for cytochrome oxidase subunit two (CO II) and the single-copy nuclear gene for calmodulin were compared among strains of Caenorhabidits elegans and two other Caenorhabditis species (C. remanei and C. briggsae). In addition the CO II sequence was determined from a distantly related nematode, Steinernema intermedii. Among the 11 strains of C. elegans tested, there are four types of CO II gene, arising from two major lineages. Levels of intraspecific difference in the CO II gene are low (less than 2.0%) compared to the extraordinary divergence between congeneric species, which is about 50% when corrected for multiple hits. Concordant with the increase in divergence between taxa is a change in the pattern of substitution from a strong transition bias (24 transitions compared to two transversions) within species to a substitution pattern that appears to reflect the base composition of the mitochondrial genome when more divergent nematodes are compared. The base composition of the Caenorhabditis CO II gene is strongly biased toward A + T at all three positions of codons and appears to constrain the amino acid composition of the protein. Both the CO II and calmodulin genes show extreme conservation of amino acid sequences. When the accumulation of changes at silent sites in the two genes is compared among strains, it becomes evident that the mitochondrial gene is changing faster than the nuclear gene.


2020 ◽  
Author(s):  
William A. Freyman ◽  
Matthew G. Johnson ◽  
Carl J. Rothfels

SummaryOrganisms such as allopolyploids and F1 hybrids contain multiple subgenomes, each potentially with its own evolutionary history. These organisms present a challenge for multilocus phylogenetic inference and other analyses since it is not apparent which gene copies from different loci are from the same subgenome.Here we introduce homologizer, a flexible Bayesian approach that uses a phylogenetic framework to infer the phasing of gene copies across loci into polyploid subgenomes.Through the use of simulation tests we demonstrate that homologizer is robust to a wide range of factors, such as the phylogenetic informativeness of loci and incomplete lineage sorting. Furthermore, we establish the utility of homologizer on real data, by analyzing a multilocus dataset consisting of nine diploids and 19 tetraploids from the fern family Cystopteridaceae.Finally, we describe how homologizer may potentially be used beyond its core phasing functionality to identify non-homologous sequences, such as hidden paralogs, contaminants, or allelic variation that was erroneously modelled as homeologous.


2020 ◽  
Vol 113 (6) ◽  
pp. 2890-2899
Author(s):  
Cheng-Lung Tsai ◽  
Hsien-Chung Lee ◽  
Geonho Cho ◽  
Yi-Chang Liao ◽  
Man-Miao Yang ◽  
...  

Abstract Pear psyllids are major pests and the causal agents of pear decline disease in orchards. In the past two decades, their outbreaks have raised issues pertaining to invasions and taxonomic identification of the dimorphic Cacopsylla chinensis (Yang and Li) in East Asia. The present study elucidated, as an aid to quarantine management, the invasive origins, differentiation history, and putative gene flow and hybridization between C. chinensis and its sibling species Cacopsylla jukyungi (Kwon). Analyses revealed that the ancestors of C. jukyungi might have diverged from C. chinensis approximately 3.5 million yr ago (Mya) and that differentiation between C. chinensis lineages I and II probably occurred 1.5 Mya. The known overlapping distribution of C. chinensis and C. jukyungi in northeastern China and the two C. chinensis lineages in the Bohai Rim region and Taiwan could be attributed to recent population expansion after the Last Glacial Maximum and/or anthropogenic activities. Analyses of the nuclear gene demonstrated that frequent gene flow between the two C. chinensis lineages and the paraphyletic relationship between C. chinensis and C. jukyungi might be caused by incomplete lineage sorting or hybridization events. On the basis of the current distribution, it is evident that C. jukyungi is not present in middle-southern China, whereas C. chinensis is not distributed in Japan and Korea. Preventing new invasions of Cacopsylla psyllids among geographic regions through the transportation of pear scions is thus pivotal in East Asia, particularly for the possible genetic exchanges among differentiated lineages after secondary invasion events.


2020 ◽  
Author(s):  
Hong-Xin Wang ◽  
Diego F. Morales-Briones ◽  
Michael J. Moore ◽  
Jun Wen ◽  
Hua-Feng Wang

AbstractThe 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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