scholarly journals Interspecific Gene Flow and the Evolution of Specialization in Black and White Rhinoceros

2020 ◽  
Vol 37 (11) ◽  
pp. 3105-3117 ◽  
Author(s):  
Yoshan Moodley ◽  
Michael V Westbury ◽  
Isa-Rita M Russo ◽  
Shyam Gopalakrishnan ◽  
Andrinajoro Rakotoarivelo ◽  
...  

Abstract Africa’s black (Diceros bicornis) and white (Ceratotherium simum) rhinoceros are closely related sister-taxa that evolved highly divergent obligate browsing and grazing feeding strategies. Although their precursor species Diceros praecox and Ceratotherium mauritanicum appear in the fossil record ∼5.2 Ma, by 4 Ma both were still mixed feeders, and were even spatiotemporally sympatric at several Pliocene sites in what is today Africa’s Rift Valley. Here, we ask whether or not D. praecox and C. mauritanicum were reproductively isolated when they came into Pliocene secondary contact. We sequenced and de novo assembled the first annotated black rhinoceros reference genome and compared it with available genomes of other black and white rhinoceros. We show that ancestral gene flow between D. praecox and C. mauritanicum ceased sometime between 3.3 and 4.1 Ma, despite conventional methods for the detection of gene flow from whole genome data returning false positive signatures of recent interspecific migration due to incomplete lineage sorting. We propose that ongoing Pliocene genetic exchange, for up to 2 My after initial divergence, could have potentially hindered the development of obligate feeding strategies until both species were fully reproductively isolated, but that the more severe and shifting paleoclimate of the early Pleistocene was likely the ultimate driver of ecological specialization in African rhinoceros.

2018 ◽  
Author(s):  
Andrinajoro R Rakotoarivelo ◽  
Yoshan Moodley

Background. The bushbuck, Tragelaphus scriptus, is the most widespread and ecologically diverse ungulate species complex within the spiral-horned antelopes, occurring in approximately 73% of the total land area of sub-Saharan Africa. This species was found to consist of two genetically divergent lineages based on the mitochondrial (mt)DNA control region. One lineage inhabited the north-western half of the African continent (T. scriptus) while the other lineage (T. sylvaticus) was found in the south-eastern half. The complex was also found to comprise an unprecedented example of 23 phylogenetically distinct groups (‘ecotypes’), with montane and desert phenotypes potentially resulting from convergent evolution. The current study aim to test hypotheses regarding historical demography and adaptation of bushbuck using a higher-resolution framework, with faster evolving nuclear markers(MGF, PRKCI, SPTBN, and THY) as well as three further mitochondrial markers (cytochrome b, 12S rRNA, and 16S rRNA). Methods. Genealogies were reconstructed for the nuclear and mitochondrial data sets and for each gene independently to test the non-monphyly of the bushbuck complexe in a multi loci framework. In addition, we reconstruct the phylogeographic history of the bushbuck complex by a Bayesian discrete phylogeographic approach of our nucDNA data set to investigate its geographic diffusion and ancestral sequence location. Results. We uncovered two evolutionarily divergent lineages and geographically restricted lineages (Sylvaticus and Scriptus) of bushbuck using phylogenetics. Molecular dating indicates that these lineages last shared a common ancestor ∼2.54 million years ago. Summary statistics and analysis of the frequency distributions of DNA polymorphisms do not have any support for expanding population. Both BSPs and EBSPs indicate that the Scriptus and Sylvaticus lineages have remained relatively stable during the last 225-450Kya. Discussion. Both nucDNA and mtDNA support previously findings of two genetically divergent Sylvaticus and Scriptus lineages, despite them coming into secondary contact in several geographic regions. The three mtDNA loci confirmed 15 of the previously defined ecotypes, including those with convergent phenotypes. However, the nuclear tree showed less phylogenetic resolution at the more derived parts of the genealogy, possibly due to incomplete lineage sorting of the slower evolving nuclear genome. The only exception to this was the montane ecotype meneliki of the Ethiopian highlands, which formed a monophyletic group at three of the four nucDNA loci. The independent evolution of this group relative to phenotypically similar montane ecotypes in Africa confirm previously suggestions of convergence within the bushbuck complex.


2021 ◽  
Author(s):  
Zheng Li ◽  
Jie Zhou ◽  
Minzhi Gao ◽  
Wei Liang ◽  
Lu Dong

Background: Understanding speciation has long been a fundamental goal of evolutionary biology. It is widely accepted that speciation requires an interruption of gene flow to generate strong reproductive isolation between species, in which sexual selection may play an important role by generating and maintaining sexual dimorphism. The mechanism of how sexual selection operated in speciation with gene flow remains an open question and the subject of many research. Two species in genus Chrysolophus, Golden pheasant (C. pictus) and Lady Amherst's pheasant (C. amherstiae), which both exhibit significant plumage dichromatism, are currently parapatric in the southwest China with several hybrid recordings in field. Methods: In this research, we estimated the pattern of gene flow during the speciation of two pheasants using the Approximate Bayesian Computation (ABC) method based on the multiple genes data. With a new assembled de novo genome of Lady Amherst's pheasant and resequencing of widely distributed individuals, we reconstructed the demographic history of the two pheasants by pairwise sequentially Markovian coalescent (PSMC). Results: The results provide clear evidence that the gene flow between the two pheasants were consistent with the prediction of isolation with migration model for allopatric populations, indicating that there was long-term gene flow after the initially divergence (ca. 2.2 million years ago), and further support the secondary contact when included the parapatric populations since around 30 ka ongoing gene flow to now, which might be induced by the population expansion of the Golden pheasant in late Pleistocene. Conclusions: The results of the study support the scenario of speciation between Golden pheasant (C. pictus) and Lady Amherst's pheasant (C. amherstiae) with cycles of mixing-isolation-mixing due to the dynamics of natural selection and sexual selection in late Pleistocene that provide a good research system as evolutionary model to test reinforcement selection in speciation. Keywords: Golden pheasant (Chrysolophus pictus), Lady Amherst's pheasant (Chrysolophus amherstiae), speciation, gene flow, Approximate Bayesian Computation (ABC), Pairwise Sequentially Markovian coalescent (PSMC).


Science ◽  
2019 ◽  
Vol 366 (6465) ◽  
pp. 594-599 ◽  
Author(s):  
Nathaniel B. Edelman ◽  
Paul B. Frandsen ◽  
Michael Miyagi ◽  
Bernardo Clavijo ◽  
John Davey ◽  
...  

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.


2021 ◽  
Author(s):  
Vanina Tonzo ◽  
AdriÀ Bellvert ◽  
Joaquín Ortego

AbstractInferring the ecological and evolutionary processes underlying lineage and phenotypic diversification is of paramount importance to shed light on the origin of contemporary patterns of biological diversity. However, reconstructing phylogenetic relationships in recent evolutionary radiations represents a major challenge due to the frequent co-occurrence of incomplete lineage sorting and introgression. In this study, we combined high throughput sequence data (ddRADseq), geometric morphometric information, and novel phylogenetic inference methods that explicitly account for gene flow to infer the evolutionary relationships and the timing and mode of diversification in a complex of Ibero-Maghrebian montane grasshoppers of the subgenus Dreuxius (genus Omocestus). Our analyses supported the phenotypic distinctiveness of most sister taxa, two events of historical introgression involving lineages at different stages of the diversification continuum, and the recent Pleistocene origin (< 1 Ma) of the complex. Phylogenetic analyses did not recover the reciprocal monophyly of taxa from Iberia and northwestern Africa, supporting overseas migration between the two continents during the Pleistocene. Collectively, these results indicate that periods of isolation and secondary contact linked to Pleistocene glacial cycles likely contributed to both allopatric speciation and post divergence gene flow in the complex. This study exemplifies how the integration of multiple lines of evidence can help to reconstruct complex histories of reticulated evolution and highlights the important role of Quaternary climatic oscillations as a diversification engine in the Ibero-Maghrebian biodiversity hotspot.


2014 ◽  
Author(s):  
Jared A Grummer ◽  
Martha L. Calderón ◽  
Adrián Nieto Montes-de Oca ◽  
Eric N Smith ◽  
Fausto Méndez-de la Cruz ◽  
...  

Interspecific gene flow is pervasive throughout the tree of life. Although detecting gene flow between populations has been facilitated by new analytical approaches, determining the timing and geography of hybridization has remained difficult, particularly for historical gene flow. A geographically explicit phylogenetic approach is needed to determine the ancestral population overlap. In this study, we performed population genetic analyses, species delimitation, simulations, and a recently developed approach of species tree diffusion to infer the phylogeographic history, timing and geographic extent of gene flow in lizards of the Sceloporus spinosus group. The two species in this group, S. spinosus and S. horridus, are distributed in eastern and western portions of Mexico, respectively, but populations of these species are sympatric in the southern Mexican highlands. We generated data consisting of three mitochondrial genes and eight nuclear loci for 148 and 68 individuals, respectively. We delimited six lineages in this group, but found strong evidence of mito-nuclear discordance in sympatric populations of S. spinosus and S. horridus owing to mitochondrial introgression. We used coalescent simulations to differentiate ancestral gene flow from secondary contact, but found mixed support for these two models. Bayesian phylogeography indicated more than 60% range overlap between ancestral S. spinosus and S. horridus populations since the time of their divergence. Isolation-migration analyses, however, revealed near-zero levels of gene flow between these ancestral populations. Interpreting results from both simulations and empirical data indicate that despite a long history of sympatry among these two species, gene flow in this group has only recently occurred.


2018 ◽  
Author(s):  
Andrinajoro R Rakotoarivelo ◽  
Paul O'Donoghue ◽  
Michael W Bruford ◽  
Yoshan Moodley

Background. The bushbuck, Tragelaphus scriptus, is the most widespread and ecologically diverse ungulate species complex within the spiral-horned antelopes. This species was recently found to consist of two genetically divergent but monophyletic Scriptus and Sylvaticus lineages, which are paraphyletic at mitochondrial (mt)DNA owing to an ancient interspecific hybridization event. The Scriptus lineage inhabits the north-western half of the African continent while Sylvaticus is found in the south-eastern half. Here we test hypotheses of historical demography and adaptation in bushbuck using a higher-resolution framework, with four nuclear (MGF, PRKCI, SPTBN, and THY) and three new mitochondrial markers (cytochrome b, 12S rRNA, and 16S rRNA). Methods. Genealogies were reconstructed for the mitochondrial and nuclear data sets, with the latter dated using fossil calibration points. We also inferred the demographic history of Scriptus and Sylvaticus using coalescent-based methods. To obtain an overview of the origins and ancestral colonisation routes of ancestral bushbuck sequences across geographic space, we conducted a discrete Bayesian phylogeographic analysis on our nuclear DNA data set. Results. Both nDNA and mtDNA support previously findings of two genetically divergent Sylvaticus and Scriptus lineages, with no allele sharing despite coming into secondary contact at several geographic locations. The three mtDNA loci confirmed 15 of the previously defined ecotypes, including those with convergent phenotypes. However, the nuclear tree showed less phylogenetic resolution at the more derived parts of the genealogy, possibly due to incomplete lineage sorting of the slower evolving nuclear genome. The only exception to this was the montane ecotype meneliki (Sylvaticus) of the Ethiopian highlands, which formed a monophyletic group at three of four nDNA loci. We dated the coalescence of the two lineages to a common ancestor ∼2.54 million years ago. Both marker sets revealed similar demographic histories of constant population size over time. We show that the bushbuck likely originated in North-East Africa, with Scriptus colonising suitable habitats towards west of the rift and Sylvaticus diffusing from east of the rift into southern Africa. Discussion. Despite lower levels of genetic structure at nuclear loci, we confirmed the independent evolution of the Menelik’s bushbuck relative to the phenotypically similar montane ecotypes in East Africa, adding further weight to previous suggestions of convergent evolution within the bushbuck complex. Perhaps the most surprising result of our analysis was that both Scriptus and Sylvaticus populations remained relatively constant throughout the Pleistocene, which is remarkable given that this was a period of major climatic and tectonic change in Africa, and responsible for driving the evolution of much of the continents extant large mammal diversity.


2018 ◽  
Author(s):  
Andrinajoro R Rakotoarivelo ◽  
Paul O'Donoghue ◽  
Michael W Bruford ◽  
Yoshan Moodley

Background. The bushbuck, Tragelaphus scriptus, is the most widespread and ecologically diverse ungulate species complex within the spiral-horned antelopes. This species was recently found to consist of two genetically divergent but monophyletic Scriptus and Sylvaticus lineages, which are paraphyletic at mitochondrial (mt)DNA owing to an ancient interspecific hybridization event. The Scriptus lineage inhabits the north-western half of the African continent while Sylvaticus is found in the south-eastern half. Here we test hypotheses of historical demography and adaptation in bushbuck using a higher-resolution framework, with four nuclear (MGF, PRKCI, SPTBN, and THY) and three new mitochondrial markers (cytochrome b, 12S rRNA, and 16S rRNA). Methods. Genealogies were reconstructed for the mitochondrial and nuclear data sets, with the latter dated using fossil calibration points. We also inferred the demographic history of Scriptus and Sylvaticus using coalescent-based methods. To obtain an overview of the origins and ancestral colonisation routes of ancestral bushbuck sequences across geographic space, we conducted a discrete Bayesian phylogeographic analysis on our nuclear DNA data set. Results. Both nDNA and mtDNA support previously findings of two genetically divergent Sylvaticus and Scriptus lineages, with no allele sharing despite coming into secondary contact at several geographic locations. The three mtDNA loci confirmed 15 of the previously defined ecotypes, including those with convergent phenotypes. However, the nuclear tree showed less phylogenetic resolution at the more derived parts of the genealogy, possibly due to incomplete lineage sorting of the slower evolving nuclear genome. The only exception to this was the montane ecotype meneliki (Sylvaticus) of the Ethiopian highlands, which formed a monophyletic group at three of four nDNA loci. We dated the coalescence of the two lineages to a common ancestor ∼2.54 million years ago. Both marker sets revealed similar demographic histories of constant population size over time. We show that the bushbuck likely originated in North-East Africa, with Scriptus colonising suitable habitats towards west of the rift and Sylvaticus diffusing from east of the rift into southern Africa. Discussion. Despite lower levels of genetic structure at nuclear loci, we confirmed the independent evolution of the Menelik’s bushbuck relative to the phenotypically similar montane ecotypes in East Africa, adding further weight to previous suggestions of convergent evolution within the bushbuck complex. Perhaps the most surprising result of our analysis was that both Scriptus and Sylvaticus populations remained relatively constant throughout the Pleistocene, which is remarkable given that this was a period of major climatic and tectonic change in Africa, and responsible for driving the evolution of much of the continents extant large mammal diversity.


2019 ◽  
Author(s):  
Xuejing Wang ◽  
Kathryn H. Maher ◽  
Nan Zhang ◽  
Pingjia Que ◽  
Chenqing Zheng ◽  
...  

AbstractUnderstanding how incipient species are maintained with gene flow is a fundamental question in evolutionary biology. Whole genome sequencing of multiple individuals holds great potential to illustrate patterns of genomic differentiation as well as the associated evolutionary histories. Kentish (Charadrius alexandrinus) and the white-faced (C. dealbatus) plovers, which differ in their phenotype, ecology and behaviour, are two incipient species and parapatrically distributed in East Asia. Previous studies show evidence of genetic diversification with gene flow between the two plovers. Under this scenario, it is of great importance to explore the patterns of divergence at the genomic level and to determine whether specific regions are involved in reproductive isolation and local adaptation. Here we present the first population genomic analysis of the two incipient species based on the de novo Kentish plover reference genome and resequenced populations. We show that the two plover lineages are distinct in both nuclear and mitochondrial genomes. Using model-based coalescence analysis, we found that population sizes of Kentish plover increased whereas white-faced plovers declined during the Last Glaciation Period. Moreover, the two plovers diverged allopatrically, with gene flow occurring after secondary contact. This has resulted in low levels of genome-wide differentiation, although we found evidence of a few highly differentiated genomic regions in both the autosomes and the Z-chromosome. This study illustrates that incipient shorebird species with gene flow after secondary contact can exhibit discrete divergence at specific genomic regions and provides basis to further exploration on the genetic basis of relevant phenotypic traits.


2020 ◽  
Author(s):  
Liming Cai ◽  
Zhenxiang Xi ◽  
Emily Moriarty Lemmon ◽  
Alan R Lemmon ◽  
Austin Mast ◽  
...  

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.


The Auk ◽  
2019 ◽  
Vol 136 (4) ◽  
Author(s):  
Catalina Palacios ◽  
Silvana García-R ◽  
Juan Luis Parra ◽  
Andrés M Cuervo ◽  
F Gary Stiles ◽  
...  

Abstract Ecological speciation can proceed despite genetic interchange when selection counteracts the homogenizing effects of migration. We tested predictions of this divergence-with-gene-flow model in Coeligena helianthea and C. bonapartei, 2 parapatric Andean hummingbirds with marked plumage divergence. We sequenced putatively neutral markers (mitochondrial DNA [mtDNA] and nuclear ultraconserved elements [UCEs]) to examine genetic structure and gene flow, and a candidate gene (MC1R) to assess its role underlying divergence in coloration. We also tested the prediction of Gloger’s rule that darker forms occur in more humid environments, and examined morphological variation to assess adaptive mechanisms potentially promoting divergence. Genetic differentiation between species was low in both ND2 and UCEs. Coalescent estimates of migration were consistent with divergence with gene flow, but we cannot reject incomplete lineage sorting reflecting recent speciation as an explanation for patterns of genetic variation. MC1R variation was unrelated to phenotypic differences. Species did not differ in macroclimatic niches but were distinct in morphology. Although we reject adaptation to variation in macroclimatic conditions as a cause of divergence, speciation may have occurred in the face of gene flow driven by other ecological pressures or by sexual selection. Marked phenotypic divergence with no neutral genetic differentiation is remarkable for Neotropical birds, and makes C. helianthea and C. bonapartei an appropriate system in which to search for the genetic basis of species differences employing genomics.


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