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BMC Evolutionary Biology[JOURNAL]

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Complete mitochondrial genome of Iniistius trivittatus and unique variation in two observed inserts between rRNA and tRNA genes in wrasses.

Liu D, Zhang Y, Zhang M … +2 more , Yang J, Tang W

BMC Evol Biol · 2020 Sep · PMID 32957913 · Full text

BACKGROUND: The family Labridae made up of 519 species in the world. The functional evolution of the feeding-related jaws leaded to differentiation of species, and the pharyngeal jaw apparatus evolved independently, but... BACKGROUND: The family Labridae made up of 519 species in the world. The functional evolution of the feeding-related jaws leaded to differentiation of species, and the pharyngeal jaw apparatus evolved independently, but evolutionary mechanism still remain unaddressed in wrasses. Mitogenomes data can be used to infer genetic diversification and investigate evolutionary history of wrasses, whereas only eight complete mitogenomes in this family have been sequenced to date. Here, we sequenced the complete mitogenomes of Iniistius trivittatus to investigate genetic differentiation among wrasse species. RESULTS: We sequenced the complete mitogenomes of I. trivittatus using a novel PCR strategy. The I. trivittatus mitogenomes is 16,820 bp in length and includes 13 protein -coding genes, 2 ribosomal RNA (rRNA) genes, 22 transfer RNA (tRNA) genes, and a control region. Compared to eight known mitochondrial genome, 2 additional noncoding regions (lengths of 121 and 107 bp), or so-called inserts, are found in the intergenic regions 12S rRNA - tRNA - 16S rRNA. The presumed origin of the two rare inserts is from tRNA- related retrotransposons. Compared with cytochrome b gene, the two insert sequences are highly conserved at the intraspecies level, but they showed significant variation and low similarity (< 70%) at the interspecies level. The insert events were only observed in I. trivittatus by checking the phylogenetic trees based on the complete mitogenomes of Labrida species. This finding provides evidence that in the mitogenomes, retrotransposon inserts result in intraspecific homoplasmy and interspecific heteroplasmy by natural selection and adaptation to various environments. CONCLUSIONS: This study found additional mitogenome inserts limited in wrasse species. The rRNA genes with inserts might have experienced a selective pressure for adaptation to feeding modes. Such knowledge can enable a better understanding of molecular mechanism underlying morphological evolution in wrasses.

Fossil-calibrated molecular phylogeny of atlantid heteropods (Gastropoda, Pterotracheoidea).

Wall-Palmer D, Janssen AW, Goetze E … +3 more , Choo LQ, Mekkes L, Peijnenburg KTCA

BMC Evol Biol · 2020 Sep · PMID 32957910 · Full text

BACKGROUND: The aragonite shelled, planktonic gastropod family Atlantidae (shelled heteropods) is likely to be one of the first groups to be impacted by imminent ocean changes, including ocean warming and ocean acidifica... BACKGROUND: The aragonite shelled, planktonic gastropod family Atlantidae (shelled heteropods) is likely to be one of the first groups to be impacted by imminent ocean changes, including ocean warming and ocean acidification. With a fossil record spanning at least 100 Ma, atlantids have experienced and survived global-scale ocean changes and extinction events in the past. However, the diversification patterns and tempo of evolution in this family are largely unknown. RESULTS: Based on a concatenated maximum likelihood phylogeny of three genes (cytochrome c oxidase subunit 1 mitochondrial DNA, 28S and 18S ribosomal rRNA) we show that the three extant genera of the family Atlantidae, Atlanta, Protatlanta and Oxygyrus, form monophyletic groups. The genus Atlanta is split into two groups, one exhibiting smaller, well ornamented shells, and the other having larger, less ornamented shells. The fossil record, in combination with a fossil-calibrated phylogeny, suggests that large scale atlantid extinction was accompanied by considerable and rapid diversification over the last 25 Ma, potentially driven by vicariance events. CONCLUSIONS: Now confronted with a rapidly changing modern ocean, the ability of atlantids to survive past global change crises gives some optimism that they may be able to persist through the Anthropocene.

Meiotic recombination in the offspring of Microbotryum hybrids and its impact on pathogenicity.

Bueker B, Guerreiro MA, Hood ME … +3 more , Brachmann A, Rahmann S, Begerow D

BMC Evol Biol · 2020 Sep · PMID 32942986 · Full text

BACKGROUND: Hybridization is a central mechanism in evolution, producing new species or introducing important genetic variation into existing species. In plant-pathogenic fungi, adaptation and specialization to exploit a... BACKGROUND: Hybridization is a central mechanism in evolution, producing new species or introducing important genetic variation into existing species. In plant-pathogenic fungi, adaptation and specialization to exploit a host species are key determinants of evolutionary success. Here, we performed experimental crosses between the two pathogenic Microbotryum species, M. lychnidis-dioicae and M. silenes-acaulis that are specialized to different hosts. The resulting offspring were analyzed on phenotypic and genomic levels to describe genomic characteristics of hybrid offspring and genetic factors likely involved in host-specialization. RESULTS: Genomic analyses of interspecific fungal hybrids revealed that individuals were most viable if the majority of loci were inherited from one species. Interestingly, species-specific loci were strictly controlled by the species' origin of the mating type locus. Moreover we detected signs of crossing over and chromosome duplications in the genomes of the analyzed hybrids. In Microbotryum, mitochondrial DNA was found to be uniparentally inherited from the a mating type. Genome comparison revealed that most gene families are shared and the majority of genes are conserved between the two species, indicating very similar biological features, including infection and pathogenicity processes. Moreover, we detected 211 candidate genes that were retained under host-driven selection of backcrossed lines. These genes and might therefore either play a crucial role in host specialization or be linked to genes that are essential for specialization. CONCLUSION: The combination of genome analyses with experimental selection and hybridization is a promising way to investigate host-pathogen interactions. This study manifests genetic factors of host specialization that are required for successful biotrophic infection of the post-zygotic stage, but also demonstrates the strong influence of intra-genomic conflicts or instabilities on the viability of hybrids in the haploid host-independent stage.

Multi-model seascape genomics identifies distinct environmental drivers of selection among sympatric marine species.

Nielsen ES, Henriques R, Beger M … +2 more , Toonen RJ, von der Heyden S

BMC Evol Biol · 2020 Sep · PMID 32938400 · Full text

BACKGROUND: As global change and anthropogenic pressures continue to increase, conservation and management increasingly needs to consider species' potential to adapt to novel environmental conditions. Therefore, it is im... BACKGROUND: As global change and anthropogenic pressures continue to increase, conservation and management increasingly needs to consider species' potential to adapt to novel environmental conditions. Therefore, it is imperative to characterise the main selective forces acting on ecosystems, and how these may influence the evolutionary potential of populations and species. Using a multi-model seascape genomics approach, we compare putative environmental drivers of selection in three sympatric southern African marine invertebrates with contrasting ecology and life histories: Cape urchin (Parechinus angulosus), Common shore crab (Cyclograpsus punctatus), and Granular limpet (Scutellastra granularis). RESULTS: Using pooled (Pool-seq), restriction-site associated DNA sequencing (RAD-seq), and seven outlier detection methods, we characterise genomic variation between populations along a strong biogeographical gradient. Of the three species, only S. granularis showed significant isolation-by-distance, and isolation-by-environment driven by sea surface temperatures (SST). In contrast, sea surface salinity (SSS) and range in air temperature correlated more strongly with genomic variation in C. punctatus and P. angulosus. Differences were also found in genomic structuring between the three species, with outlier loci contributing to two clusters in the East and West Coasts for S. granularis and P. angulosus, but not for C. punctatus. CONCLUSION: The findings illustrate distinct evolutionary potential across species, suggesting that species-specific habitat requirements and responses to environmental stresses may be better predictors of evolutionary patterns than the strong environmental gradients within the region. We also found large discrepancies between outlier detection methodologies, and thus offer a novel multi-model approach to identifying the principal environmental selection forces acting on species. Overall, this work highlights how adding a comparative approach to seascape genomics (both with multiple models and species) can elucidate the intricate evolutionary responses of ecosystems to global change.

Genotypic similarities among the parthenogenetic Darevskia rock lizards with different hybrid origins.

Tarkhnishvili D, Yanchukov A, Şahin MK … +14 more , Gabelaia M, Murtskhvaladze M, Candan K, Galoyan E, Arakelyan M, Iankoshvili G, Kumlutaş Y, Ilgaz Ç, Matur F, Çolak F, Erdolu M, Kurdadze S, Barateli N, Anderson CL

BMC Evol Biol · 2020 Sep · PMID 32938384 · Full text

BACKGROUND: The majority of parthenogenetic vertebrates derive from hybridization between sexually reproducing species, but the exact number of hybridization events ancestral to currently extant clonal lineages is diffic... BACKGROUND: The majority of parthenogenetic vertebrates derive from hybridization between sexually reproducing species, but the exact number of hybridization events ancestral to currently extant clonal lineages is difficult to determine. Usually, we do not know whether the parental species are able to contribute their genes to the parthenogenetic vertebrate lineages after the initial hybridization. In this paper, we address the hypothesis, whether some genotypes of seven phenotypically distinct parthenogenetic rock lizards (genus Darevskia) could have resulted from back-crosses of parthenogens with their presumed parental species. We also tried to identify, as precise as possible, the ancestral populations of all seven parthenogens. RESULTS: We analysed partial mtDNA sequences and microsatellite genotypes of all seven parthenogens and their presumed ansectral species, sampled across the entire geographic range of parthenogenesis in this group. Our results confirm the previous designation of the parental species, but further specify the maternal populations that are likely ancestral to different parthenogenetic lineages. Contrary to the expectation of independent hybrid origins of the unisexual taxa, we found that genotypes at multiple loci were shared frequently between different parthenogenetic species. The highest proportions of shared genotypes were detected between (i) D. sapphirina and D. bendimahiensis and (ii) D. dahli and D. armeniaca, and less often between other parthenogens. In case (ii), genotypes at the remaining loci were notably distinct. CONCLUSIONS: We suggest that both observations (i-ii) can be explained by two parthenogenetic forms tracing their origin to a single initial hybridization event. In case (ii), however, occasional gene exchange between the unisexual and the parental bisexual species could have taken place after the onset of parthenogenetic reproduction. Indeed, backcrossed polyploid hybrids are relatively frequent in Darevskia, although no direct evidence of recent gene flow has been previously documented. Our results further suggest that parthenogens are losing heterozygosity as a result of allelic conversion, hence their fitness is expected to decline over time as genetic diversity declines. Backcrosses with the parental species could be a rescue mechanism which might prevent this decline, and therefore increase the persistance of unisexual forms.

Further resolution of the house mouse (Mus musculus) phylogeny by integration over isolation-with-migration histories.

Phifer-Rixey M, Harr B, Hey J

BMC Evol Biol · 2020 Sep · PMID 32933487 · Full text

BACKGROUND: The three main subspecies of house mice, Mus musculus castaneus, Mus musculus domesticus, and Mus musculus musculus, are estimated to have diverged ~ 350-500KYA. Resolution of the details of their evolutionar... BACKGROUND: The three main subspecies of house mice, Mus musculus castaneus, Mus musculus domesticus, and Mus musculus musculus, are estimated to have diverged ~ 350-500KYA. Resolution of the details of their evolutionary history is complicated by their relatively recent divergence, ongoing gene flow among the subspecies, and complex demographic histories. Previous studies have been limited to some extent by the number of loci surveyed and/or by the scope of the method used. Here, we apply a method (IMa3) that provides an estimate of a population phylogeny while allowing for complex histories of gene exchange. RESULTS: Results strongly support a topology with M. m. domesticus as sister to M. m. castaneus and M. m. musculus. In addition, we find evidence of gene flow between all pairs of subspecies, but that gene flow is most restricted from M. m. musculus into M. m. domesticus. Estimates of other key parameters are dependent on assumptions regarding generation time and mutation rate in house mice. Nevertheless, our results support previous findings that the effective population size, N of M. m. castaneus is larger than that of the other two subspecies, that the three subspecies began diverging ~ 130 - 420KYA, and that the time between divergence events was short. CONCLUSIONS: Joint demographic and phylogenetic analyses of genomic data provide a clearer picture of the history of divergence in house mice.

Similar patterns of genetic diversity and linkage disequilibrium in Western chimpanzees (Pan troglodytes verus) and humans indicate highly conserved mechanisms of MHC molecular evolution.

Vangenot C, Nunes JM, Doxiadis GM … +4 more , Poloni ES, Bontrop RE, de Groot NG, Sanchez-Mazas A

BMC Evol Biol · 2020 Sep · PMID 32933484 · Full text

BACKGROUND: Many species are threatened with extinction as their population sizes decrease with changing environments or face novel pathogenic threats. A reduction of genetic diversity at major histocompatibility complex... BACKGROUND: Many species are threatened with extinction as their population sizes decrease with changing environments or face novel pathogenic threats. A reduction of genetic diversity at major histocompatibility complex (MHC) genes may have dramatic effects on populations' survival, as these genes play a key role in adaptive immunity. This might be the case for chimpanzees, the MHC genes of which reveal signatures of an ancient selective sweep likely due to a viral epidemic that reduced their population size a few million years ago. To better assess how this past event affected MHC variation in chimpanzees compared to humans, we analysed several indexes of genetic diversity and linkage disequilibrium across seven MHC genes on four cohorts of chimpanzees and we compared them to those estimated at orthologous HLA genes in a large set of human populations. RESULTS: Interestingly, the analyses uncovered similar patterns of both molecular diversity and linkage disequilibrium across the seven MHC genes in chimpanzees and humans. Indeed, in both species the greatest allelic richness and heterozygosity were found at loci A, B, C and DRB1, the greatest nucleotide diversity at loci DRB1, DQA1 and DQB1, and both significant global linkage disequilibrium and the greatest proportions of haplotypes in linkage disequilibrium were observed at pairs DQA1 ~ DQB1, DQA1 ~ DRB1, DQB1 ~ DRB1 and B ~ C. Our results also showed that, despite some differences among loci, the levels of genetic diversity and linkage disequilibrium observed in contemporary chimpanzees were globally similar to those estimated in small isolated human populations, in contrast to significant differences compared to large populations. CONCLUSIONS: We conclude, first, that highly conserved mechanisms shaped the diversity of orthologous MHC genes in chimpanzees and humans. Furthermore, our findings support the hypothesis that an ancient demographic decline affecting the chimpanzee populations - like that ascribed to a viral epidemic - exerted a substantial effect on the molecular diversity of their MHC genes, albeit not more pronounced than that experienced by HLA genes in human populations that underwent rapid genetic drift during humans' peopling history. We thus propose a model where chimpanzees' MHC genes regenerated molecular variation through recombination/gene conversion and/or balancing selection after the selective sweep.

The development of early pioneer neurons in the annelid Malacoceros fuliginosus.

Kumar S, Tumu SC, Helm C … +1 more , Hausen H

BMC Evol Biol · 2020 Sep · PMID 32928118 · Full text

BACKGROUND: Nervous system development is an interplay of many processes: the formation of individual neurons, which depends on whole-body and local patterning processes, and the coordinated growth of neurites and synaps... BACKGROUND: Nervous system development is an interplay of many processes: the formation of individual neurons, which depends on whole-body and local patterning processes, and the coordinated growth of neurites and synapse formation. While knowledge of neural patterning in several animal groups is increasing, data on pioneer neurons that create the early axonal scaffold are scarce. Here we studied the first steps of nervous system development in the annelid Malacoceros fuliginosus. RESULTS: We performed a dense expression profiling of a broad set of neural genes. We found that SoxB expression begins at 4 h postfertilization, and shortly later, the neuronal progenitors can be identified at the anterior and the posterior pole by the transient and dynamic expression of proneural genes. At 9 hpf, the first neuronal cells start differentiating, and we provide a detailed description of axonal outgrowth of the pioneer neurons that create the primary neuronal scaffold. Tracing back the clonal origin of the ventral nerve cord pioneer neuron revealed that it is a descendant of the blastomere 2d (2d), which after 7 cleavages starts expressing Neurogenin, Acheate-Scute and NeuroD. CONCLUSIONS: We propose that an anterior and posterior origin of the nervous system is ancestral in annelids. We suggest that closer examination of the first pioneer neurons will be valuable in better understanding of nervous system development in spirally cleaving animals, to determine the potential role of cell-intrinsic properties in neuronal specification and to resolve the evolution of nervous systems.

Testing species hypotheses for Fridericia magna, an enchytraeid worm (Annelida: Clitellata) with great mitochondrial variation.

Martinsson S, Klinth M, Erséus C

BMC Evol Biol · 2020 Sep · PMID 32928097 · Full text

BACKGROUND: Deep mitochondrial divergences were observed in Scandinavian populations of the terrestrial to semi-aquatic annelid Fridericia magna (Clitellata: Enchytraeidae). This raised the need for testing whether the t... BACKGROUND: Deep mitochondrial divergences were observed in Scandinavian populations of the terrestrial to semi-aquatic annelid Fridericia magna (Clitellata: Enchytraeidae). This raised the need for testing whether the taxon is a single species or a complex of cryptic species. RESULTS: A total of 62 specimens from 38 localities were included in the study, 44 of which were used for species delimitation. First, the 44 specimens were divided into clusters using ABGD (Automatic Barcode Gap Discovery) on two datasets, consisting of sequences of the mitochondrial markers COI and 16S. For each dataset, the worms were divided into six not completely congruent clusters. When they were combined, a maximum of seven clusters, or species hypotheses, were obtained, and the seven clusters were used as input in downstream analyses. We tested these hypotheses by constructing haplowebs for two nuclear markers, H3 and ITS, and in both haplowebs the specimens appeared as a single species. Multi-locus species delimitation analyses performed with the Bayesian BPP program also mainly supported a single species. Furthermore, no apparent morphological differences were found between the clusters. Two of the clusters were partially separated from each other and the other clusters, but not strongly enough to consider them as separate species. All 62 specimens were used to visualise the Scandinavian distribution, of the species, and to compare with published COI data from other Fridericia species. CONCLUSION: We show that the morphospecies Fridericia magna is a single species, harbouring several distinct mitochondrial clusters. There is partial genetic separation between some of them, which may be interpreted as incipient speciation. The study shows the importance of rigorous species delimitation using several independent markers when deep mitochondrial divergences might give the false impression of cryptic speciation.

The speciation and adaptation of the polyploids: a case study of the Chinese Isoetes L. diploid-polyploid complex.

Dai X, Li X, Huang Y … +1 more , Liu X

BMC Evol Biol · 2020 Sep · PMID 32928096 · Full text

BACKGROUND: The Chinese Isoetes L. are distributed in a stairway pattern: diploids in the high altitude and polyploids in the low altitude. The allopolyploid I. sinensis and its diploid parents I. yunguiensis and I. taiw... BACKGROUND: The Chinese Isoetes L. are distributed in a stairway pattern: diploids in the high altitude and polyploids in the low altitude. The allopolyploid I. sinensis and its diploid parents I. yunguiensis and I. taiwanensis is an ideal system with which to investigate the relationships between polyploid speciation and the ecological niches preferences. RESULTS: There were two major clades in the nuclear phylogenetic tree, all of the populations of polyploid were simultaneously located in both clades. The chloroplast phylogenetic tree included two clades with different populations of the polyploid clustered with the diploids separately: I. yunguiensis with partial populations of the I. sinensis and I. taiwanensis with the rest populations of the I. sinensis. The crow node of the I. sinensis allopolyploid system was 4.43 Ma (95% HPD: 2.77-6.97 Ma). The divergence time between I. sinensis and I. taiwanensis was estimated to 0.65 Ma (95% HPD: 0.26-1.91 Ma). The narrower niche breadth in I.sinensis than those of its diploid progenitors and less niche overlap in the pairwise comparisons between the polyploid and its progenitors. CONCLUSIONS: Our results elucidate that I. yunguinensis and I. taiwanensis contribute to the speciation of I. sinensis, the diploid parents are the female parents of different populations. The change of altitude might have played an important role in allopolyploid speciation and the pattern of distribution of I. sinensis. Additionally, niche novelty of the allopolyploid population of I. sinensis has been detected, in accordance with the hypothesis that niche shift between the polyploids and its diploid progenitors is important for the establishment and persistence of the polyploids.

Species delimitation in the cyanolichen genus Rostania.

Košuthová A, Bergsten J, Westberg M … +1 more , Wedin M

BMC Evol Biol · 2020 Sep · PMID 32912146 · Full text

BACKGROUND: In this study, we investigate species limits in the cyanobacterial lichen genus Rostania (Collemataceae, Peltigerales, Lecanoromycetes). Four molecular markers (mtSSU rDNA, β-tubulin, MCM7, RPB2) were sequenc... BACKGROUND: In this study, we investigate species limits in the cyanobacterial lichen genus Rostania (Collemataceae, Peltigerales, Lecanoromycetes). Four molecular markers (mtSSU rDNA, β-tubulin, MCM7, RPB2) were sequenced and analysed with two coalescent-based species delimitation methods: the Generalized Mixed Yule Coalescent model (GMYC) and a Bayesian species delimitation method (BPP) using a multispecies coalescence model (MSC), the latter with or without an a priori defined guide tree. RESULTS: Species delimitation analyses indicate the presence of eight strongly supported candidate species. Conclusive correlation between morphological/ecological characters and genetic delimitation could be found for six of these. Of the two additional candidate species, one is represented by a single sterile specimen and the other currently lacks morphological or ecological supporting evidence. CONCLUSIONS: We conclude that Rostania includes a minimum of six species: R. ceranisca, R. multipunctata, R. occultata 1, R. occultata 2, R. occultata 3, and R. occultata 4,5,6. Three distinct Nostoc morphotypes occur in Rostania, and there is substantial correlation between these morphotypes and Rostania thallus morphology.

Allelic diversity and patterns of selection at the major histocompatibility complex class I and II loci in a threatened shorebird, the Snowy Plover (Charadrius nivosus).

Cruz-López M, Fernández G, Hipperson H … +8 more , Palacios E, Cavitt J, Galindo-Espinosa D, Gómez Del Angel S, Pruner R, Gonzalez O, Burke T, Küpper C

BMC Evol Biol · 2020 Sep · PMID 32912143 · Full text

BACKGROUND: Understanding the structure and variability of adaptive loci such as the major histocompatibility complex (MHC) genes is a primary research goal for evolutionary and conservation genetics. Typically, classica... BACKGROUND: Understanding the structure and variability of adaptive loci such as the major histocompatibility complex (MHC) genes is a primary research goal for evolutionary and conservation genetics. Typically, classical MHC genes show high polymorphism and are under strong balancing selection, as their products trigger the adaptive immune response in vertebrates. Here, we assess the allelic diversity and patterns of selection for MHC class I and class II loci in a threatened shorebird with highly flexible mating and parental care behaviour, the Snowy Plover (Charadrius nivosus) across its broad geographic range. RESULTS: We determined the allelic and nucleotide diversity for MHC class I and class II genes using samples of 250 individuals from eight breeding population of Snowy Plovers. We found 40 alleles at MHC class I and six alleles at MHC class II, with individuals carrying two to seven different alleles (mean 3.70) at MHC class I and up to two alleles (mean 1.45) at MHC class II. Diversity was higher in the peptide-binding region, which suggests balancing selection. The MHC class I locus showed stronger signatures of both positive and negative selection than the MHC class II locus. Most alleles were present in more than one population. If present, private alleles generally occurred at very low frequencies in each population, except for the private alleles of MHC class I in one island population (Puerto Rico, lineage tenuirostris). CONCLUSION: Snowy Plovers exhibited an intermediate level of diversity at the MHC, similar to that reported in other Charadriiformes. The differences found in the patterns of selection between the class I and II loci are consistent with the hypothesis that different mechanisms shape the sequence evolution of MHC class I and class II genes. The rarity of private alleles across populations is consistent with high natal and breeding dispersal and the low genetic structure previously observed at neutral genetic markers in this species.

Potential causes and consequences of rapid mitochondrial genome evolution in thermoacidophilic Galdieria (Rhodophyta).

Cho CH, Park SI, Ciniglia C … +4 more , Yang EC, Graf L, Bhattacharya D, Yoon HS

BMC Evol Biol · 2020 Sep · PMID 32892741 · Full text

BACKGROUND: The Cyanidiophyceae is an early-diverged red algal class that thrives in extreme conditions around acidic hot springs. Although this lineage has been highlighted as a model for understanding the biology of ex... BACKGROUND: The Cyanidiophyceae is an early-diverged red algal class that thrives in extreme conditions around acidic hot springs. Although this lineage has been highlighted as a model for understanding the biology of extremophilic eukaryotes, little is known about the molecular evolution of their mitochondrial genomes (mitogenomes). RESULTS: To fill this knowledge gap, we sequenced five mitogenomes from representative clades of Cyanidiophyceae and identified two major groups, here referred to as Galdieria-type (G-type) and Cyanidium-type (C-type). G-type mitogenomes exhibit the following three features: (i) reduction in genome size and gene inventory, (ii) evolution of unique protein properties including charge, hydropathy, stability, amino acid composition, and protein size, and (iii) distinctive GC-content and skewness of nucleotides. Based on GC-skew-associated characteristics, we postulate that unidirectional DNA replication may have resulted in the rapid evolution of G-type mitogenomes. CONCLUSIONS: The high divergence of G-type mitogenomes was likely driven by natural selection in the multiple extreme environments that Galdieria species inhabit combined with their highly flexible heterotrophic metabolism. We speculate that the interplay between mitogenome divergence and adaptation may help explain the dominance of Galdieria species in diverse extreme habitats.

Genomic differentiation across the speciation continuum in three hummingbird species pairs.

Henderson EC, Brelsford A

BMC Evol Biol · 2020 Sep · PMID 32883209 · Full text

BACKGROUND: The study of speciation has expanded with the increasing availability and affordability of high-resolution genomic data. How the genome evolves throughout the process of divergence and which regions of the ge... BACKGROUND: The study of speciation has expanded with the increasing availability and affordability of high-resolution genomic data. How the genome evolves throughout the process of divergence and which regions of the genome are responsible for causing and maintaining that divergence have been central questions in recent work. Here, we use three pairs of species from the recently diverged bee hummingbird clade to investigate differences in the genome at different stages of speciation, using divergence times as a proxy for the speciation continuum. RESULTS: Population measures of relative differentiation between hybridizing species reveal that different chromosome types diverge at different stages of speciation. Using F as our relative measure of differentiation we found that the sex chromosome shows signs of divergence early in speciation. Next, small autosomes (microchromosomes) accumulate highly diverged genomic regions, while the large autosomes (macrochromosomes) accumulate genomic regions of divergence at a later stage of speciation. CONCLUSIONS: Our finding that genomic windows of elevated F accumulate on small autosomes earlier in speciation than on larger autosomes is counter to the prediction that F increases with size of chromosome (i.e. with decreased recombination rate), and is not represented when weighted average F per chromosome is compared with chromosome size. The results of this study suggest that multiple chromosome characteristics such as recombination rate and gene density combine to influence the genomic locations of signatures of divergence.

Dynamics behind disjunct distribution, hotspot-edge refugia, and discordant RADseq/mtDNA variability: insights from the Emei mustache toad.

Zheng Y, Dai Q, Guo X … +1 more , Zeng X

BMC Evol Biol · 2020 Aug · PMID 32859147 · Full text

BACKGROUND: The distribution of genetic diversity and the underlying processes are important for conservation planning but are unknown for most species and have not been well studied in many regions. In East Asia, the Si... BACKGROUND: The distribution of genetic diversity and the underlying processes are important for conservation planning but are unknown for most species and have not been well studied in many regions. In East Asia, the Sichuan Basin and surrounding mountains constitute an understudied region that exhibits a "ring" of high species richness overlapping the eastern edge of the global biodiversity hotspot Mountains of Southwest China. We examine the distributional history and genetic diversification of the Emei mustache toad Leptobrachium boringii, a typical "ring" element characterized by disjunct ranges in the mountains, by integrating time-calibrated gene tree, genetic variability, individual-level clustering, inference of population splitting and mixing from allele frequencies, and paleoclimatic suitability modeling. RESULTS: The results reveal extensive range dynamics, including secondary contact after long-term isolation via westward dispersal accompanied by variability loss. They allow the proposal of a model that combines recurrent contractions caused by Quaternary climatic changes and some failed expansions under suitable conditions for explaining the shared disjunct distribution pattern. Providing exceptional low-elevation habitats in the hotspot area, the eastern edge harbors both long-term refugial and young immigrant populations. This finding and a synthesis of evidence from other taxa demonstrate that a certain contributor to biodiversity, one that preserves and receives low-elevation elements of the east in this case, can be significant for only a particular part of a hotspot. By clarifying the low variability of these refugial populations, we show that discordant mitochondrial estimates of diversity can be obtained for populations that experienced admixture, which would have unlikely left proportional immigrant alleles for each locus. CONCLUSIONS: Dispersal after long-term isolation can explain much of the spatial distribution of genetic diversity in this species, while secondary contact and long-term persistence do not guarantee a large variation. The model for the formation of disjunct ranges may apply to many other taxa isolated in the mountains surrounding the Sichuan Basin. Furthermore, this study provides insights into the heterogeneous nature of hotspots and discordant variability obtained from genome-wide and mitochondrial data.

The roles of vicariance and isolation by distance in shaping biotic diversification across an ancient archipelago: evidence from a Seychelles caecilian amphibian.

Maddock ST, Nussbaum RA, Day JJ … +7 more , Latta L, Miller M, Fisk DL, Wilkinson M, Rocha S, Gower DJ, Pfrender ME

BMC Evol Biol · 2020 Aug · PMID 32847507 · Full text

BACKGROUND: Island systems offer excellent opportunities for studying the evolutionary histories of species by virtue of their restricted size and easily identifiable barriers to gene flow. However, most studies investig... BACKGROUND: Island systems offer excellent opportunities for studying the evolutionary histories of species by virtue of their restricted size and easily identifiable barriers to gene flow. However, most studies investigating evolutionary patterns and processes shaping biotic diversification have focused on more recent (emergent) rather than ancient oceanic archipelagos. Here, we focus on the granitic islands of the Seychelles, which are unusual among island systems because they have been isolated for a long time and are home to a monophyletic radiation of caecilian amphibians that has been separated from its extant sister lineage for ca. 65-62 Ma. We selected the most widespread Seychelles caecilian species, Hypogeophis rostratus, to investigate intraspecific morphological and genetic (mitochondrial and nuclear) variation across the archipelago (782 samples from nine islands) to identify patterns and test processes that shaped their evolutionary history within the Seychelles. RESULTS: Overall a signal of strong geographic structuring with distinct northern- and southern-island clusters were identified across all datasets. We suggest that these distinct groups have been isolated for ca. 1.26 Ma years without subsequent migration between them. Populations from the somewhat geographically isolated island of Frégate showed contrasting relationships to other islands based on genetic and morphological data, clustering alternatively with northern-island (genetic) and southern-island (morphological) populations. CONCLUSIONS: Although variation in H. rostratus across the Seychelles is explained more by isolation-by-distance than by adaptation, the genetic-morphological incongruence for affinities of Frégate H. rostratus might be caused by local adaptation over-riding the signal from their vicariant history. Our findings highlight the need of integrative approaches to investigate fine-scale geographic structuring to uncover underlying diversity and to better understand evolutionary processes on ancient, continental islands.

Unlocking a signal of introgression from codons in Lachancea kluyveri using a mutation-selection model.

Landerer C, O'Meara BC, Zaretzki R … +1 more , Gilchrist MA

BMC Evol Biol · 2020 Aug · PMID 32842959 · Full text

BACKGROUND: For decades, codon usage has been used as a measure of adaptation for translational efficiency and translation accuracy of a gene's coding sequence. These patterns of codon usage reflect both the selective an... BACKGROUND: For decades, codon usage has been used as a measure of adaptation for translational efficiency and translation accuracy of a gene's coding sequence. These patterns of codon usage reflect both the selective and mutational environment in which the coding sequences evolved. Over this same period, gene transfer between lineages has become widely recognized as an important biological phenomenon. Nevertheless, most studies of codon usage implicitly assume that all genes within a genome evolved under the same selective and mutational environment, an assumption violated when introgression occurs. In order to better understand the effects of introgression on codon usage patterns and vice versa, we examine the patterns of codon usage in Lachancea kluyveri, a yeast which has experienced a large introgression. We quantify the effects of mutation bias and selection for translation efficiency on the codon usage pattern of the endogenous and introgressed exogenous genes using a Bayesian mixture model, ROC SEMPPR, which is built on mechanistic assumptions about protein synthesis and grounded in population genetics. RESULTS: We find substantial differences in codon usage between the endogenous and exogenous genes, and show that these differences can be largely attributed to differences in mutation bias favoring A/T ending codons in the endogenous genes while favoring C/G ending codons in the exogenous genes. Recognizing the two different signatures of mutation bias and selection improves our ability to predict protein synthesis rate by 42% and allowed us to accurately assess the decaying signal of endogenous codon mutation and preferences. In addition, using our estimates of mutation bias and selection, we identify Eremothecium gossypii as the closest relative to the exogenous genes, providing an alternative hypothesis about the origin of the exogenous genes, estimate that the introgression occurred ∼6×10 generation ago, and estimate its historic and current selection against mismatched codon usage. CONCLUSIONS: Our work illustrates how mechanistic, population genetic models like ROC SEMPPR can separate the effects of mutation and selection on codon usage and provide quantitative estimates from sequence data.

Investigation of mechanisms underlying chaotic genetic patchiness in the intertidal marbled crab Pachygrapsus marmoratus (Brachyura: Grapsidae) across the Ligurian Sea.

Iannucci A, Cannicci S, Caliani I … +3 more , Baratti M, Pretti C, Fratini S

BMC Evol Biol · 2020 Aug · PMID 32831022 · Full text

BACKGROUND: Studies on marine community dynamics and population structures are limited by the lack of exhaustive knowledge on the larval dispersal component of connectivity. Genetic data represents a powerful tool in und... BACKGROUND: Studies on marine community dynamics and population structures are limited by the lack of exhaustive knowledge on the larval dispersal component of connectivity. Genetic data represents a powerful tool in understanding such processes in the marine realm. When dealing with dispersion and connectivity in marine ecosystems, many evidences show patterns of genetic structure that cannot be explained by any clear geographic trend and may show temporal instability. This scenario is usually referred to as chaotic genetic patchiness, whose driving mechanisms are recognized to be selection, temporal shifts in local population dynamics, sweepstakes reproductive success and collective dispersal. In this study we focused on the marbled crab Pachygrapsus marmoratus that inhabits the rocky shores of the Mediterranean Sea, Black Sea and East Atlantic Ocean, and disperses through planktonic larvae for about 1 month. P. marmoratus exhibits unexpectedly low connectivity levels at local scale, although well-defined phylogeographic patterns across the species' distribution range were described. This has been explained as an effect of subtle geographic barriers or due to sweepstake reproductive success. In order to verify a chaotic genetic patchiness scenario, and to explore mechanisms underlying it, we planned our investigation within the Ligurian Sea, an isolated basin of the western Mediterranean Sea, and we genotyped 321 individuals at 11 microsatellite loci. RESULTS: We recorded genetic heterogeneity among our Ligurian Sea samples with the occurrence of genetic clusters not matching the original populations and a slight inter-population divergence, with the geographically most distant populations being the genetically most similar ones. Moreover, individuals from each site were assigned to all the genetic clusters. We also recorded evidences of self-recruitment and a higher than expected within-site kinship. CONCLUSIONS: Overall, our results suggest that the chaotic genetic patchiness we found in P. marmoratus Ligurian Sea populations is the result of a combination of differences in reproductive success, en masse larval dispersion and local larval retention. This study defines P. marmoratus as an example of marine spawner whose genetic pool is not homogenous at population level, but rather split in a chaotic mosaic of slightly differentiated genetic patches derived from complex and dynamic ecological processes.

Revealing the diversity of amber source plants from the Early Cretaceous Crato Formation, Brazil.

Seyfullah LJ, Roberts EA, Schmidt AR … +5 more , Ragazzi E, Anderson KB, Rodrigues do Nascimento D, Ferreira da Silva Filho W, Kunzmann L

BMC Evol Biol · 2020 Aug · PMID 32819273 · Full text

BACKGROUND: Amber has been reported from the Early Cretaceous Crato Formation, as isolated clasts or within plant tissues. Undescribed cones of uncertain gymnosperm affinity have also been recovered with amber preserved... BACKGROUND: Amber has been reported from the Early Cretaceous Crato Formation, as isolated clasts or within plant tissues. Undescribed cones of uncertain gymnosperm affinity have also been recovered with amber preserved in situ. Here, we provide multiple lines of evidence to determine the botanical affinity of this enigmatic, conspicuous cone type, and to better understand the diversity of amber-source plants present in the Crato Formation and beyond. RESULTS: A new taxon of amber-bearing pollen cone Araripestrobus resinosus gen. nov. et sp. nov. is described here from complete cones and characteristic disarticulated portions. The best-preserved cone portion has both in situ amber infilling the resin canals inside the preserved microsporophyll tissues and pollen of the Eucommiidites-type. This places this genus within the Erdtmanithecales, an incompletely known gymnosperm group from the Mesozoic. FTIR analysis of the in situ amber indicates a potential araucariacean conifer affinity, although affinity with cupressacean conifers cannot be definitely ruled out. Pyr-GC-MS analysis of the Araripestrobus resinosus gen. nov. et sp. nov. in situ fossil resin shows that it is a mature class Ib amber, thought to indicate affinities with araucariacean and cupressacean, but not pinaceous, conifers. This is the first confirmed occurrence of this class of amber in the Crato Formation flora and in South America, except for an archaeological sample from Laguna Guatavita, Colombia. CONCLUSIONS: The combined results of the cones' novel gross morphology and the analyses of the in situ amber and pollen clearly indicate that the new taxon of resinous gymnosperm pollen cones from the Crato Formation is affiliated with Erdtmanithecales. The cone morphology is very distinct from all known pollen cone types of this extinct plant group. We therefore assume that the plant group that produced Eucommiidites-type pollen is much more diverse in habits than previously thought. Moreover, the diversity of potential amber source plants from the Crato Formation is now expanded beyond the Araucariaceae and the Cheirolepidiaceae to include this member of the Erdtmanithecales. Despite dispersed Eucommiidites pollen being noted from the Crato Formation, this is the first time macrofossils of Erdtmanithecales have been recognized from the Early Cretaceous of South America.

Rapid size change associated with intra-island evolutionary radiation in extinct Caribbean "island-shrews".

Woods R, Turvey ST, Brace S … +5 more , McCabe CV, Dalén L, Rayfield EJ, Brown MJF, Barnes I

BMC Evol Biol · 2020 Aug · PMID 32811443 · Full text

BACKGROUND: The Caribbean offers a unique opportunity to study evolutionary dynamics in insular mammals. However, the recent extinction of most Caribbean non-volant mammals has obstructed evolutionary studies, and poor D... BACKGROUND: The Caribbean offers a unique opportunity to study evolutionary dynamics in insular mammals. However, the recent extinction of most Caribbean non-volant mammals has obstructed evolutionary studies, and poor DNA preservation associated with tropical environments means that very few ancient DNA sequences are available for extinct vertebrates known from the region's Holocene subfossil record. The endemic Caribbean eulipotyphlan family Nesophontidae ("island-shrews") became extinct ~ 500 years ago, and the taxonomic validity of many Nesophontes species and their wider evolutionary dynamics remain unclear. Here we use both morphometric and palaeogenomic methods to clarify the status and evolutionary history of Nesophontes species from Hispaniola, the second-largest Caribbean island. RESULTS: Principal component analysis of 65 Nesophontes mandibles from late Quaternary fossil sites across Hispaniola identified three non-overlapping morphometric clusters, providing statistical support for the existence of three size-differentiated Hispaniolan Nesophontes species. We were also able to extract and sequence ancient DNA from a ~ 750-year-old specimen of Nesophontes zamicrus, the smallest non-volant Caribbean mammal, including a whole-mitochondrial genome and partial nuclear genes. Nesophontes paramicrus (39-47 g) and N. zamicrus (~ 10 g) diverged recently during the Middle Pleistocene (mean estimated divergence = 0.699 Ma), comparable to the youngest species splits in Eulipotyphla and other mammal groups. Pairwise genetic distance values for N. paramicrus and N. zamicrus based on mitochondrial and nuclear genes are low, but fall within the range of comparative pairwise data for extant eulipotyphlan species-pairs. CONCLUSIONS: Our combined morphometric and palaeogenomic analyses provide evidence for multiple co-occurring species and rapid body size evolution in Hispaniolan Nesophontes, in contrast to patterns of genetic and morphometric differentiation seen in Hispaniola's extant non-volant land mammals. Different components of Hispaniola's mammal fauna have therefore exhibited drastically different rates of morphological evolution. Morphological evolution in Nesophontes is also rapid compared to patterns across the Eulipotyphla, and our study provides an important new example of rapid body size change in a small-bodied insular vertebrate lineage. The Caribbean was a hotspot for evolutionary diversification as well as preserving ancient biodiversity, and studying the surviving representatives of its mammal fauna is insufficient to reveal the evolutionary patterns and processes that generated regional diversity.
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