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BMC Evolutionary Biology[JOURNAL]

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Adaptive divergence in shell morphology in an ongoing gastropod radiation from Lake Malawi.

Van Bocxlaer B, Ortiz-Sepulveda CM, Gurdebeke PR … +1 more , Vekemans X

BMC Evol Biol · 2020 Jan · PMID 31918659 · Full text

BACKGROUND: Ecological speciation is a prominent mechanism of diversification but in many evolutionary radiations, particularly in invertebrates, it remains unclear whether supposedly critical ecological traits drove or... BACKGROUND: Ecological speciation is a prominent mechanism of diversification but in many evolutionary radiations, particularly in invertebrates, it remains unclear whether supposedly critical ecological traits drove or facilitated diversification. As a result, we lack accurate knowledge on the drivers of diversification for most evolutionary radiations along the tree of life. Freshwater mollusks present an enigmatic example: Putatively adaptive radiations are being described in various families, typically from long-lived lakes, whereas other taxa represent celebrated model systems in the study of ecophenotypic plasticity. Here we examine determinants of shell-shape variation in three nominal species of an ongoing ampullariid radiation in the Malawi Basin (Lanistes nyassanus, L. solidus and Lanistes sp. (ovum-like)) with a common garden experiment and semi-landmark morphometrics. RESULTS: We found significant differences in survival and fecundity among these species in contrasting habitats. Morphological differences observed in the wild persisted in our experiments for L. nyassanus versus L. solidus and L. sp. (ovum-like), but differences between L. solidus and L. sp. (ovum-like) disappeared and re-emerged in the F and F generations, respectively. These results indicate that plasticity occurred, but that it is not solely responsible for the observed differences. Our experiments provide the first unambiguous evidence for genetic divergence in shell morphology in an ongoing freshwater gastropod radiation in association with marked fitness differences among species under controlled habitat conditions. CONCLUSIONS: Our results indicate that differences in shell morphology among Lanistes species occupying different habitats have an adaptive value. These results also facilitate an accurate reinterpretation of morphological variation in fossil Lanistes radiations, and thus macroevolutionary dynamics. Finally, our work testifies that the shells of freshwater gastropods may retain signatures of adaptation at low taxonomic levels, beyond representing an evolutionary novelty responsible for much of the diversity and disparity in mollusks altogether.

Fossils from South China redefine the ancestral euarthropod body plan.

Aria C, Zhao F, Zeng H … +2 more , Guo J, Zhu M

BMC Evol Biol · 2020 Jan · PMID 31914921 · Full text

BACKGROUND: Early Cambrian Lagerstätten from China have greatly enriched our perspective on the early evolution of animals, particularly arthropods. However, recent studies have shown that many of these early fossil arth... BACKGROUND: Early Cambrian Lagerstätten from China have greatly enriched our perspective on the early evolution of animals, particularly arthropods. However, recent studies have shown that many of these early fossil arthropods were more derived than previously thought, casting uncertainty on the ancestral euarthropod body plan. In addition, evidence from fossilized neural tissues conflicts with external morphology, in particular regarding the homology of the frontalmost appendage. RESULTS: Here we redescribe the multisegmented megacheirans Fortiforceps and Jianfengia and describe Sklerolibyon maomima gen. et sp. nov., which we place in Jianfengiidae, fam. nov. (in Megacheira, emended). We find that jianfengiids show high morphological diversity among megacheirans, both in trunk ornamentation and head anatomy, which encompasses from 2 to 4 post-frontal appendage pairs. These taxa are also characterized by elongate podomeres likely forming seven-segmented endopods, which were misinterpreted in their original descriptions. Plesiomorphic traits also clarify their connection with more ancestral taxa. The structure and position of the "great appendages" relative to likely sensory antero-medial protrusions, as well as the presence of optic peduncles and sclerites, point to an overall homology with the anterior head of radiodontans. This is confirmed by our Bayesian phylogeny, which places jianfengiids as the basalmost euarthropods, paraphyletic with other megacheirans, and in contiguity with isoxyids and radiodontans. CONCLUSIONS: Sklerolibyon and other jianfengiids expand the disparity of megacheirans and suggest that the common euarthropod ancestor possessed a remarkable phenotypic variability associated with the externalized cephalon, as well as endopods that were already heptopodomerous, which differs from previous hypotheses and observations. These animals also demonstrate that the frontalmost pair of arthrodized appendage is homologous between radiodontans and megacheirans, refuting the claim that the radiodontan frontal appendages evolved into the euarthropod labrum, and questioning its protocerebral identity. This evidence based on external anatomy now constitutes a solid benchmark upon which we should address issues of homology, with the help of carefully examined palaeoneurological data.

Living on the edge: comparative phylogeography and phylogenetics of Oreohelix land snails at their range edge in Western Canada.

Dempsey ZW, Goater CP, Burg TM

BMC Evol Biol · 2020 Jan · PMID 31906912 · Full text

BACKGROUND: The biodiversity and distributions of terrestrial snails at local and regional scales are influenced by their low vagility and microhabitat specificity. The accessibility of large-bodied species and their cha... BACKGROUND: The biodiversity and distributions of terrestrial snails at local and regional scales are influenced by their low vagility and microhabitat specificity. The accessibility of large-bodied species and their characteristically high levels of genetic polymorphism make them excellent ecological and evolutionary models for studies on the phylogeography, phylogenetics, and conservation of organisms in fragmented populations. This study aims to elucidate the biodiversity, systematics, and distributions of genetic lineages within the genus Oreohelix at the northern and western periphery of their range. RESULTS: We found four mitochondrial clades, three of which are putative subspecies of Oreohelix subrudis. One clade was geographically widespread, occurring within numerous sites in Cypress Hills and in the Rocky Mountains, a second was geographically restricted to the Rocky Mountains in Alberta, and a third was restricted to the Cypress Hills region. A fourth clade was the small-bodied species, O. cooperi. ITS2 sequence and screening data revealed three genetic clusters, of which one was O. cooperi. Cluster 1 contained most individuals in COI clade X and some from clade B and cluster 2 was predominantly made up of individuals from COI clades B and B' and a few from clade X. ITS2 alleles were shared in a narrow contact zone between two COI clades, suggestive of hybridization between the two. CONCLUSIONS: A sky island known as Cypress Hills, in southeastern Alberta, Canada, is a biodiversity hotspot for terrestrial land snails in the genus Oreohelix. The observed phylogeographic patterns likely reflect reproductive isolation during the Last Glacial Maximum, followed by secondary contact due to passive, long-range dispersal resulting from low vagility, local adaptation, and complex glacial history.

Genetic diversity of a widespread annual killifish from coastal Tanzania.

Bartáková V, Nagy B, Polačik M … +3 more , Blažek R, Lamtane H, Reichard M

BMC Evol Biol · 2020 Jan · PMID 31906845 · Full text

BACKGROUND: African annual killifishes (Nothobranchius spp.) are adapted to seasonally desiccating habitats (ephemeral pools), surviving dry periods as dormant eggs. Given their peculiar life history, geographic aspects... BACKGROUND: African annual killifishes (Nothobranchius spp.) are adapted to seasonally desiccating habitats (ephemeral pools), surviving dry periods as dormant eggs. Given their peculiar life history, geographic aspects of their diversity uniquely combine patterns typical for freshwater taxa (river basin structure and elevation gradient) and terrestrial animals (rivers acting as major dispersal barriers). However, our current knowledge on fine-scale inter-specific and intra-specific genetic diversity of African annual fish is limited to a single, particularly dry region of their distribution (subtropical Mozambique). Using a widespread annual killifish from coastal Tanzania and Kenya, we tested whether the same pattern of genetic divergence pertains to a wet equatorial region in the centre of Nothobranchius distribution. RESULTS: In populations of Nothobranchius melanospilus species group across its range, we genotyped a part of mitochondrial cytochrome oxidase subunit 1 (COI) gene (83 individuals from 22 populations) and 10 nuclear microsatellite markers (251 individuals from 16 populations). We found five lineages with a clear phylogeographic structure but frequent secondary contact. Mitochondrial lineages were largely congruent with main population genetic clusters identified on microsatellite markers. In the upper Wami basin, populations are isolated as a putative Nothobranchius prognathus, but include also a population from a periphery of the middle Ruvu basin. Other four lineages (including putative Nothobranchius kwalensis) coexisted in secondary contact zones, but possessed clear spatial pattern. Main river channels did not form apparent barriers to dispersal. The most widespread lineage had strong signal of recent population expansion. CONCLUSIONS: We conclude that dispersal of a Nothobranchius species from a wet part of the genus distribution (tropical lowland) is not constrained by main river channels and closely related lineages frequently coexist in secondary contact zones. We also demonstrate contemporary connection between the Ruvu and Rufiji river basins. Our data do not provide genetic support for existence of recently described cryptic species from N. melanospilus complex, but cannot resolve this issue.

Characterizing the ribosomal tandem repeat and its utility as a DNA barcode in lichen-forming fungi.

Bradshaw M, Grewe F, Thomas A … +6 more , Harrison CH, Lindgren H, Muggia L, St Clair LL, Lumbsch HT, Leavitt SD

BMC Evol Biol · 2020 Jan · PMID 31906844 · Full text

BACKGROUND: Regions within the nuclear ribosomal operon are a major tool for inferring evolutionary relationships and investigating diversity in fungi. In spite of the prevalent use of ribosomal markers in fungal researc... BACKGROUND: Regions within the nuclear ribosomal operon are a major tool for inferring evolutionary relationships and investigating diversity in fungi. In spite of the prevalent use of ribosomal markers in fungal research, central features of nuclear ribosomal DNA (nrDNA) evolution are poorly characterized for fungi in general, including lichenized fungi. The internal transcribed spacer (ITS) region of the nrDNA has been adopted as the primary DNA barcode identification marker for fungi. However, little is known about intragenomic variation in the nrDNA in symbiotic fungi. In order to better understand evolution of nrDNA and the utility of the ITS region for barcode identification of lichen-forming fungal species, we generated nearly complete nuclear ribosomal operon sequences from nine species in the Rhizoplaca melanophthalma species complex using short reads from high-throughput sequencing. RESULTS: We estimated copy numbers for the nrDNA operon, ranging from nine to 48 copies for members of this complex, and found low levels of intragenomic variation in the standard barcode region (ITS). Monophyly of currently described species in this complex was supported in phylogenetic inferences based on the ITS, 28S, intergenic spacer region, and some intronic regions, independently; however, a phylogenetic inference based on the 18S provided much lower resolution. Phylogenetic analysis of concatenated ITS and intergenic spacer sequence data generated from 496 specimens collected worldwide revealed previously unrecognized lineages in the nrDNA phylogeny. CONCLUSIONS: The results from our study support the general assumption that the ITS region of the nrDNA is an effective barcoding marker for fungi. For the R. melanophthalma group, the limited amount of potential intragenomic variability in the ITS region did not correspond to fixed diagnostic nucleotide position characters separating taxa within this species complex. Previously unrecognized lineages inferred from ITS sequence data may represent undescribed species-level lineages or reflect uncharacterized aspects of nrDNA evolution in the R. melanophthalma species complex.

Molecular differentiation of the Murraya paniculata Complex (Rutaceae: Aurantioideae: Aurantieae).

Nguyen CH, Beattie GAC, Haigh AM … +4 more , Astuti IP, Mabberley DJ, Weston PH, Holford P

BMC Evol Biol · 2019 Dec · PMID 31888450 · Full text

BACKGROUND: Orange jasmine has a complex nomenclatural history and is now known as Murraya paniculata (L.) Jack. Our interest in this common ornamental stemmed from the need to resolve its identity and the identities of... BACKGROUND: Orange jasmine has a complex nomenclatural history and is now known as Murraya paniculata (L.) Jack. Our interest in this common ornamental stemmed from the need to resolve its identity and the identities of closely related taxa as hosts of the pathogen 'Candidatus Liberibacter asiaticus' and its vector Diaphorina citri. Understanding these microbe-vector-plant relationships has been hampered by taxonomic confusion surrounding Murraya at both the generic and specific levels. RESULTS: To resolve the taxonomic uncertainty, six regions of the maternally-inherited chloroplastal genome and part of the nuclear-encoded ITS region were amplified from 85 accessions of Murraya and Merrillia using the polymerase chain reaction (PCR). Clustering used maximum parsimony (MP), maximum likelihood (ML) and Bayesian inference (BI). Chronograms were produced for molecular dating, and to test the monophyly of Murraya rigorously, using selected accessions of Murraya and 26 accessions of the Rutaceae and Simarubaceae. Sequence data from the ITS and chloroplastal regions suggest that Murraya paniculata (sensu (Swingle WT and Reece CR, The Citrus Industry, p. 190-430, 1967)) can be separated into four distinct but morphologically somewhat cryptic taxa: Murraya paniculata (sensu (Mabberley DJ, Taxon 65:366-371, 2016)), M. elongata, M. sumatrana and M. lucida. In addition, Murraya omphalocarpa was identified as a putative hybrid of M. paniculata and M. lucida with two geographically isolated nothovarieties representing reciprocal crosses. Murraya is monophyletic, and molecular dating suggests that it diverged from Merrillia during the Miocene (23-5 Ma) with this Murraya group speciating and dispersing during the Middle Miocene onwards. CONCLUSIONS: The accessions from Asia and Australasia used in this study grouped into biogeographical regions that match herbarium specimen records for the taxa that suggest natural allopatric distributions with limited overlap and hybridity. Murraya paniculata has been distributed around the world as an ornamental plant. The division of the Murraya paniculata complex into four species with a rare hybrid also confirms morphological studies.

The geography of evolutionary divergence in the highly endemic avifauna from the Sierra Madre del Sur, Mexico.

Rocha-Méndez A, Sánchez-González LA, González C … +1 more , Navarro-Sigüenza AG

BMC Evol Biol · 2019 Dec · PMID 31888449 · Full text

BACKGROUND: Mesoamerica is a remarkable region with a high geological and ecological complexity. Within northern Mesoamerica, the biotic province of the Sierra Madre del Sur (SMS) in southwestern Mexico harbors exception... BACKGROUND: Mesoamerica is a remarkable region with a high geological and ecological complexity. Within northern Mesoamerica, the biotic province of the Sierra Madre del Sur (SMS) in southwestern Mexico harbors exceptionally high avian endemism and diversity. Herein, we searched for spatially and temporally concordant phylogeographic patterns, in four bird genera from three distinct avian orders co-distributed across Mesoamerica and investigated their causes through hypothesis testing regarding historical processes. Selected species include endemic and differentiated populations across the montane forests of Mesoamerica, and particularly within the SMS. RESULTS: We gathered mitochondrial DNA sequences for at least one locus from 177 individuals across all species. We assessed genetic structure, demographic history, and defined a framework for the coalescent simulations used in biogeographic hypothesis testing temporal and spatial co-variance. Our analyses suggested shared phylogeographic breaks in areas corresponding to the SMS populations, and between the main montane systems in Mesoamerica, with the Central Valley of Oaxaca and the Nicaragua Depression being the most frequently shared breaks among analyzed taxa. Nevertheless, dating analyses and divergence patterns observed were consistent with the hypothesis of broad vicariance across Mesoamerica derived from mechanisms operating at distinct times across taxa in the SMS. CONCLUSIONS: Our study provides a framework for understanding the evolutionary origins and historical factors enhancing speciation in well-defined regions within Mesoamerica, indicating that the evolutionary history of extant biota inhabiting montane forests is complex and often idiosyncratic.

Morphology and evolutionary significance of phosphatic otoliths within the inner ears of cartilaginous fishes (Chondrichthyes).

Schnetz L, Pfaff C, Libowitzky E … +3 more , Johanson Z, Stepanek R, Kriwet J

BMC Evol Biol · 2019 Dec · PMID 31888446 · Full text

BACKGROUND: Chondrichthyans represent a monophyletic group of crown group gnathostomes and are central to our understanding of vertebrate evolution. Like all vertebrates, cartilaginous fishes evolved concretions of mater... BACKGROUND: Chondrichthyans represent a monophyletic group of crown group gnathostomes and are central to our understanding of vertebrate evolution. Like all vertebrates, cartilaginous fishes evolved concretions of material within their inner ears to aid with equilibrium and balance detection. Up to now, these materials have been identified as calcium carbonate-bearing otoconia, which are small bio-crystals consisting of an inorganic mineral and a protein, or otoconial masses (aggregations of otoconia bound by an organic matrix), being significantly different in morphology compared to the singular, polycrystalline otolith structures of bony fishes, which are solidified bio-crystals forming stony masses. Reinvestigation of the morphological and chemical properties of these chondrichthyan otoconia revises our understanding of otolith composition and has implications on the evolution of these characters in both the gnathostome crown group, and cartilaginous fishes in particular. RESULTS: Dissections of Amblyraja radiata, Potamotrygon leopoldi, and Scyliorhinus canicula revealed three pairs of singular polycrystalline otolith structures with a well-defined morphology within their inner ears, as observed in bony fishes. IR spectroscopy identified the material to be composed of carbonate/collagen-bearing apatite in all taxa. These findings contradict previous hypotheses suggesting these otoconial structures were composed of calcium carbonate in chondrichthyans. A phylogenetic mapping using 37 chondrichthyan taxa further showed that the acquisition of phosphatic otolith structures might be widespread within cartilaginous fishes. CONCLUSIONS: Differences in the size and shape of otoliths between taxa indicate a taxonomic signal within elasmobranchs. Otoliths made of carbonate/collagen-bearing apatite are reported for the first time in chondrichthyans. The intrinsic pathways to form singular, polycrystalline otoliths may represent the plesiomorphic condition for vertebrates but needs further testing. Likewise, the phosphatic composition of otoliths in early vertebrates such as cyclostomes and elasmobranchs is probably closely related to the lack of bony tissue in these groups, supporting a close relationship between skeletal tissue mineralization patterns and chemical otolith composition, underlined by physiological constraints.

The phylogenetic significance of the morphology of the syrinx, hyoid and larynx, of the southern cassowary, Casuarius casuarius (Aves, Palaeognathae).

McInerney PL, Lee MSY, Clement AM … +1 more , Worthy TH

BMC Evol Biol · 2019 Dec · PMID 31881941 · Full text

BACKGROUND: Palaeognathae is a basal clade within Aves and include the large and flightless ratites and the smaller, volant tinamous. Although much research has been conducted on various aspects of palaeognath morphology... BACKGROUND: Palaeognathae is a basal clade within Aves and include the large and flightless ratites and the smaller, volant tinamous. Although much research has been conducted on various aspects of palaeognath morphology, ecology, and evolutionary history, there are still areas which require investigation. This study aimed to fill gaps in our knowledge of the Southern Cassowary, Casuarius casuarius, for which information on the skeletal systems of the syrinx, hyoid and larynx is lacking - despite these structures having been recognised as performing key functional roles associated with vocalisation, respiration and feeding. Previous research into the syrinx and hyoid have also indicated these structures to be valuable for determining evolutionary relationships among neognath taxa, and thus suggest they would also be informative for palaeognath phylogenetic analyses, which still exhibits strong conflict between morphological and molecular trees. RESULTS: The morphology of the syrinx, hyoid and larynx of C. casuarius is described from CT scans. The syrinx is of the simple tracheo-bronchial syrinx type, lacking specialised elements such as the pessulus; the hyoid is relatively short with longer ceratobranchials compared to epibranchials; and the larynx is comprised of entirely cartilaginous, standard avian anatomical elements including a concave, basin-like cricoid and fused cricoid wings. As in the larynx, both the syrinx and hyoid lack ossification and all three structures were most similar to Dromaius. We documented substantial variation across palaeognaths in the skeletal character states of the syrinx, hyoid, and larynx, using both the literature and novel observations (e.g. of C. casuarius). Notably, new synapomorphies linking Dinornithiformes and Tinamidae are identified, consistent with the molecular evidence for this clade. These shared morphological character traits include the ossification of the cricoid and arytenoid cartilages, and an additional cranial character, the articulation between the maxillary process of the nasal and the maxilla. CONCLUSION: Syrinx, hyoid and larynx characters of palaeognaths display greater concordance with molecular trees than do other morphological traits. These structures might therefore be less prone to homoplasy related to flightlessness and gigantism, compared to typical morphological traits emphasised in previous phylogenetic studies.

A genome-skimmed phylogeny of a widespread bryozoan family, Adeonidae.

Orr RJS, Haugen MN, Berning B … +11 more , Bock P, Cumming RL, Florence WK, Hirose M, Di Martino E, Ramsfjell MH, Sannum MM, Smith AM, Vieira LM, Waeschenbach A, Liow LH

BMC Evol Biol · 2019 Dec · PMID 31881939 · Full text

BACKGROUND: Understanding the phylogenetic relationships among species is one of the main goals of systematic biology. Simultaneously, credible phylogenetic hypotheses are often the first requirement for unveiling the ev... BACKGROUND: Understanding the phylogenetic relationships among species is one of the main goals of systematic biology. Simultaneously, credible phylogenetic hypotheses are often the first requirement for unveiling the evolutionary history of traits and for modelling macroevolutionary processes. However, many non-model taxa have not yet been sequenced to an extent such that statistically well-supported molecular phylogenies can be constructed for these purposes. Here, we use a genome-skimming approach to extract sequence information for 15 mitochondrial and 2 ribosomal operon genes from the cheilostome bryozoan family, Adeonidae, Busk, 1884, whose current systematics is based purely on morphological traits. The members of the Adeonidae are, like all cheilostome bryozoans, benthic, colonial, marine organisms. Adeonids are also geographically widely-distributed, often locally common, and are sometimes important habitat-builders. RESULTS: We successfully genome-skimmed 35 adeonid colonies representing 6 genera (Adeona, Adeonellopsis, Bracebridgia, Adeonella, Laminopora and Cucullipora). We also contributed 16 new, circularised mitochondrial genomes to the eight previously published for cheilostome bryozoans. Using the aforementioned mitochondrial and ribosomal genes, we inferred the relationships among these 35 samples. Contrary to some previous suggestions, the Adeonidae is a robustly supported monophyletic clade. However, the genera Adeonella and Laminopora are in need of revision: Adeonella is polyphyletic and Laminopora paraphyletically forms a clade with some Adeonella species. Additionally, we assign a sequence clustering identity using cox1 barcoding region of 99% at the species and 83% at the genus level. CONCLUSIONS: We provide sequence data, obtained via genome-skimming, that greatly increases the resolution of the phylogenetic relationships within the adeonids. We present a highly-supported topology based on 17 genes and substantially increase availability of circularised cheilostome mitochondrial genomes, and highlight how we can extend our pipeline to other bryozoans.

Modelling the evolution of cognitive styles.

Liedtke J, Fromhage L

BMC Evol Biol · 2019 Dec · PMID 31881934 · Full text

BACKGROUND: Individuals consistently differ in behaviour, exhibiting so-called personalities. In many species, individuals differ also in their cognitive abilities. When personalities and cognitive abilities occur in dis... BACKGROUND: Individuals consistently differ in behaviour, exhibiting so-called personalities. In many species, individuals differ also in their cognitive abilities. When personalities and cognitive abilities occur in distinct combinations, they can be described as 'cognitive styles'. Both empirical and theoretical investigations produced contradicting or mixed results regarding the complex interplay between cognitive styles and environmental conditions. RESULTS: Here we use individual-based simulations to show that, under just slightly different environmental conditions, different cognitive styles exist and under a variety of conditions, can also co-exist. Co-existences are based on individual specialization on different resources, or, more generally speaking, on individuals adopting different niches or microhabitats. CONCLUSIONS: The results presented here suggest that in many species, individuals of the same population may adopt different cognitive styles. Thereby the present study may help to explain the variety of styles described in previous studies and why different, sometimes contradicting, results have been found under similar conditions.

The ability of single genes vs full genomes to resolve time and space in outbreak analysis.

Dudas G, Bedford T

BMC Evol Biol · 2019 Dec · PMID 31878875 · Full text

BACKGROUND: Inexpensive pathogen genome sequencing has had a transformative effect on the field of phylodynamics, where ever increasing volumes of data have promised real-time insight into outbreaks of infectious disease... BACKGROUND: Inexpensive pathogen genome sequencing has had a transformative effect on the field of phylodynamics, where ever increasing volumes of data have promised real-time insight into outbreaks of infectious disease. As well as the sheer volume of pathogen isolates being sequenced, the sequencing of whole pathogen genomes, rather than select loci, has allowed phylogenetic analyses to be carried out at finer time scales, often approaching serial intervals for infections caused by rapidly evolving RNA viruses. Despite its utility, whole genome sequencing of pathogens has not been adopted universally and targeted sequencing of loci is common in some pathogen-specific fields. RESULTS: In this study we highlighted the utility of sequencing whole genomes of pathogens by re-analysing a well-characterised collection of Ebola virus sequences in the form of complete viral genomes (≈19 kb long) or the rapidly evolving glycoprotein (GP, ≈2 kb long) gene. We have quantified changes in phylogenetic, temporal, and spatial inference resolution as a result of this reduction in data and compared these to theoretical expectations. CONCLUSIONS: We propose a simple intuitive metric for quantifying temporal resolution, i.e. the time scale over which sequence data might be informative of various processes as a quick back-of-the-envelope calculation of statistical power available to molecular clock analyses.

Phenotypic plasticity of natural Populus trichocarpa populations in response to temporally environmental change in a common garden.

Liu Y, El-Kassaby YA

BMC Evol Biol · 2019 Dec · PMID 31878866 · Full text

BACKGROUND: Natural selection on fitness-related traits can be temporally heterogeneous among populations. As climate changes, understanding population-level responses is of scientific and practical importance. We examin... BACKGROUND: Natural selection on fitness-related traits can be temporally heterogeneous among populations. As climate changes, understanding population-level responses is of scientific and practical importance. We examined 18 phenotypic traits associated with phenology, biomass, and ecophysiology in 403 individuals of natural Populus trichocarpa populations, growing in a common garden. RESULTS: Compared with tree origin settings, propagules likely underwent drought exposures in the common garden due to significantly low rainfall during the years of measurement. All study traits showed population differentiation reflecting adaptive responses due to local genetic adaptation. Phenology and biomass traits were strongly under selection and showed plastic responses between years, co-varying with latitude. While phenological events (e.g., bud set and growth period) and biomass were under positive directional selection, post-bud set period, particularly from final bud set to the onset of leaf drop, was selected against. With one exception to water-use efficiency, ecophysiology traits were under negative directional selection. Moreover, extended phenological events jointly evolved with source niches under increased temperature and decreased rainfall exposures. High biomass coevolved with climatic niches of high temperature; low rainfall promoted high photosynthetic rates evolution. CONCLUSIONS: This work underpins that P. trichocarpa is likely to experience increased fitness (height gain) by evolving toward extended bud set and growth period, abbreviated post-bud set period, and increased drought resistance, potentially constituting a powerful mechanism for long-lived tree species in surviving unpredictably environmental extremes (e.g., drought).

Influence of environmental factors on the genetic variation of the aquatic macrophyte Ranunculus subrigidus on the Qinghai-Tibetan Plateau.

Wu Z, Xu X, Zhang J … +2 more , Wiegleb G, Hou H

BMC Evol Biol · 2019 Dec · PMID 31856717 · Full text

BACKGROUND: Due to the environmental heterogeneity along elevation gradients, alpine ecosystems are ideal study objects for investigating how ecological variables shape the genetic patterns of natural species. The highes... BACKGROUND: Due to the environmental heterogeneity along elevation gradients, alpine ecosystems are ideal study objects for investigating how ecological variables shape the genetic patterns of natural species. The highest region in the world, the Qinghai-Tibetan Plateau, is a hotspot for the studies of evolutionary processes in plants. Many large rivers spring from the plateau, providing abundant habitats for aquatic and amphibious organisms. In the present study, we examined the genetic diversity of 13 Ranunculus subrigidus populations distributed throughout the plateau in order to elucidate the relative contribution of geographic distance and environmental dissimilarity to the spatial genetic pattern. RESULTS: A relatively low level of genetic diversity within populations was found. No spatial genetic structure was suggested by the analyses of molecular variance, Bayesian clustering analysis and Mantel tests. Partial Mantel tests and multiple matrix regression analysis showed a significant influence of the environment on the genetic divergence of the species. Both climatic and water quality variables contribute to the habitat heterogeneity of R. subrigidus populations. CONCLUSIONS: Our results suggest that historical processes involving long-distance dispersal and local adaptation may account for the genetic patterns of R. subrigidus and current environmental factors play an important role in the genetic differentiation and local adaptation of aquatic plants in alpine landscapes.

Variability of mitochondrial ORFans hints at possible differences in the system of doubly uniparental inheritance of mitochondria among families of freshwater mussels (Bivalvia: Unionida).

Guerra D, Lopes-Lima M, Froufe E … +9 more , Gan HM, Ondina P, Amaro R, Klunzinger MW, Callil C, Prié V, Bogan AE, Stewart DT, Breton S

BMC Evol Biol · 2019 Dec · PMID 31856711 · Full text

BACKGROUND: Supernumerary ORFan genes (i.e., open reading frames without obvious homology to other genes) are present in the mitochondrial genomes of gonochoric freshwater mussels (Bivalvia: Unionida) showing doubly unip... BACKGROUND: Supernumerary ORFan genes (i.e., open reading frames without obvious homology to other genes) are present in the mitochondrial genomes of gonochoric freshwater mussels (Bivalvia: Unionida) showing doubly uniparental inheritance (DUI) of mitochondria. DUI is a system in which distinct female-transmitted and male-transmitted mitotypes coexist in a single species. In families Unionidae and Margaritiferidae, the transition from dioecy to hermaphroditism and the loss of DUI appear to be linked, and this event seems to affect the integrity of the ORFan genes. These observations led to the hypothesis that the ORFans have a role in DUI and/or sex determination. Complete mitochondrial genome sequences are however scarce for most families of freshwater mussels, therefore hindering a clear localization of DUI in the various lineages and a comprehensive understanding of the influence of the ORFans on DUI and sexual systems. Therefore, we sequenced and characterized eleven new mitogenomes from poorly sampled freshwater mussel families to gather information on the evolution and variability of the ORFan genes and their protein products. RESULTS: We obtained ten complete plus one almost complete mitogenome sequence from ten representative species (gonochoric and hermaphroditic) of families Margaritiferidae, Hyriidae, Mulleriidae, and Iridinidae. ORFan genes are present only in DUI species from Margaritiferidae and Hyriidae, while non-DUI species from Hyriidae, Iridinidae, and Mulleriidae lack them completely, independently of their sexual system. Comparisons among the proteins translated from the newly characterized ORFans and already known ones provide evidence of conserved structures, as well as family-specific features. CONCLUSIONS: The ORFan proteins show a comparable organization of secondary structures among different families of freshwater mussels, which supports a conserved physiological role, but also have distinctive family-specific features. Given this latter observation and the fact that the ORFans can be either highly mutated or completely absent in species that secondarily lost DUI depending on their respective family, we hypothesize that some aspects of the connection among ORFans, sexual systems, and DUI may differ in the various lineages of unionids.

Neutral genomic signatures of host-parasite coevolution.

Živković D, John S, Verin M … +2 more , Stephan W, Tellier A

BMC Evol Biol · 2019 Dec · PMID 31856710 · Full text

BACKGROUND: Coevolution is a selective process of reciprocal adaptation in hosts and parasites or in mutualistic symbionts. Classic population genetics theory predicts the signatures of selection at the interacting loci... BACKGROUND: Coevolution is a selective process of reciprocal adaptation in hosts and parasites or in mutualistic symbionts. Classic population genetics theory predicts the signatures of selection at the interacting loci of both species, but not the neutral genome-wide polymorphism patterns. To bridge this gap, we build an eco-evolutionary model, where neutral genomic changes over time are driven by a single selected locus in hosts and parasites via a simple biallelic gene-for-gene or matching-allele interaction. This coevolutionary process may lead to cyclic changes in the sizes of the interacting populations. RESULTS: We investigate if and when these changes can be observed in the site frequency spectrum of neutral polymorphisms from host and parasite full genome data. We show that changes of the host population size are too smooth to be observable in its polymorphism pattern over the course of time. Conversely, the parasite population may undergo a series of strong bottlenecks occurring on a slower relative time scale, which may lead to observable changes in a time series sample. We also extend our results to cases with 1) several parasites per host accelerating relative time, and 2) multiple parasite generations per host generation slowing down rescaled time. CONCLUSIONS: Our results show that time series sampling of host and parasite populations with full genome data are crucial to understand if and how coevolution occurs. This model provides therefore a framework to interpret and draw inference from genome-wide polymorphism data of interacting species.

Low adaptive potential for tolerance to ethynylestradiol, but also low toxicity, in a grayling population (Thymallus thymallus).

Marques da Cunha L, Maitre D, Wedekind C

BMC Evol Biol · 2019 Dec · PMID 31842751 · Full text

BACKGROUND: The presence of a novel pollutant can induce rapid evolution if there is additive genetic variance for the tolerance to the stressor. Continuous selection over some generations can then reduce the toxicity of... BACKGROUND: The presence of a novel pollutant can induce rapid evolution if there is additive genetic variance for the tolerance to the stressor. Continuous selection over some generations can then reduce the toxicity of the pollutant but also deplete the additive genetic variance for the tolerance and thereby slow down adaptation. One common pollutant that has been ecologically relevant for some time is 17alpha-ethynylestradiol (EE2), a synthetic compound of oral contraceptives since their market launch in the 1960s. EE2 is typically found in higher concentrations in rivers than in lakes. Recent experimental work revealed significant genetic variance for the tolerance to EE2 in two lake-spawning salmonid species but no such variance in river-spawning brown trout. We used another river-spawning salmonid, the European grayling Thymallus thymallus, to study the toxicity of an ecologically relevant concentration of EE2. We also used a full-factorial in vitro breeding design and singly rearing of 1555 embryos and larvae of 40 sib groups to test whether there is additive genetic variance for the tolerance to this pollutant. RESULTS: We found that exposure to EE2 reduced larval growth after hatching, but contrary to what has been found in the other salmonids, there were no significant effects of EE2 on embryo growth and survival. We found additive genetic variance for embryo viability, i.e. heritability for fitness. However, there was no significant additive variance for the tolerance to EE2. CONCLUSIONS: Our findings support the hypothesis that continuous selection has reduced the toxicity of EE2 and depleted genetic variance for tolerance to this synthetic stressor.

Correction to: Multiple selective sweeps of ancient polymorphisms in and around LTα located in the MHC class III region on chromosome 6.

Campbell MC, Ashong B, Teng S … +2 more , Harvey J, Cross CN

BMC Evol Biol · 2019 Dec · PMID 31842744 · Full text

After publication of our article [1] we were notified that a few duplicate sentences were included on Figure 3 and Figure 4 legends. After publication of our article [1] we were notified that a few duplicate sentences were included on Figure 3 and Figure 4 legends.

3D shape analyses of extant primate and fossil hominin vertebrae support the ancestral shape hypothesis for intervertebral disc herniation.

Plomp KA, Dobney K, Weston DA … +2 more , Strand Viðarsdóttir U, Collard M

BMC Evol Biol · 2019 Dec · PMID 31842740 · Full text

BACKGROUND: Recently we proposed an evolutionary explanation for a spinal pathology that afflicts many people, intervertebral disc herniation (Plomp et al. [2015] BMC Evolutionary Biology 15, 68). Using 2D data, we found... BACKGROUND: Recently we proposed an evolutionary explanation for a spinal pathology that afflicts many people, intervertebral disc herniation (Plomp et al. [2015] BMC Evolutionary Biology 15, 68). Using 2D data, we found that the bodies and pedicles of lower vertebrae of pathological humans were more similar in shape to those of chimpanzees than were those of healthy humans. Based on this, we hypothesized that some individuals are more prone to intervertebral disc herniation because their vertebrae exhibit ancestral traits and therefore are less well adapted for the stresses associated with bipedalism. Here, we report a study in which we tested this "Ancestral Shape Hypothesis" with 3D data from the last two thoracic and first lumbar vertebrae of pathological Homo sapiens, healthy H. sapiens, Pan troglodytes, and several extinct hominins. RESULTS: We found that the pathological and healthy H. sapiens vertebrae differed significantly in shape, and that the pathological H. sapiens vertebrae were closer in shape to the P. troglodytes vertebrae than were the healthy H. sapiens vertebrae. Additionally, we found that the pathological human vertebrae were generally more similar in shape to the vertebrae of the extinct hominins than were the healthy H. sapiens vertebrae. These results are consistent with the predictions of the Ancestral Shape Hypothesis. Several vertebral traits were associated with disc herniation, including a vertebral body that is both more circular and more ventrally wedged, relatively short pedicles and laminae, relatively long, more cranio-laterally projecting transverse processes, and relatively long, cranially-oriented spinous processes. We found that there are biomechanical and comparative anatomical reasons for suspecting that all of these traits are capable of predisposing individuals to intervertebral disc herniation. CONCLUSIONS: The results of the present study add weight to the hypothesis that intervertebral disc herniation in H. sapiens is connected with vertebral shape. Specifically, they suggest that individuals whose vertebrae are towards the ancestral end of the range of shape variation within H. sapiens have a greater propensity to develop the condition than other individuals. More generally, the study shows that evolutionary thinking has the potential to shed new light on human skeletal pathologies.

tRNA functional signatures classify plastids as late-branching cyanobacteria.

Lawrence TJ, Amrine KC, Swingley WD … +1 more , Ardell DH

BMC Evol Biol · 2019 Dec · PMID 31818253 · Full text

BACKGROUND: Eukaryotes acquired the trait of oxygenic photosynthesis through endosymbiosis of the cyanobacterial progenitor of plastid organelles. Despite recent advances in the phylogenomics of Cyanobacteria, the phylog... BACKGROUND: Eukaryotes acquired the trait of oxygenic photosynthesis through endosymbiosis of the cyanobacterial progenitor of plastid organelles. Despite recent advances in the phylogenomics of Cyanobacteria, the phylogenetic root of plastids remains controversial. Although a single origin of plastids by endosymbiosis is broadly supported, recent phylogenomic studies are contradictory on whether plastids branch early or late within Cyanobacteria. One underlying cause may be poor fit of evolutionary models to complex phylogenomic data. RESULTS: Using Posterior Predictive Analysis, we show that recently applied evolutionary models poorly fit three phylogenomic datasets curated from cyanobacteria and plastid genomes because of heterogeneities in both substitution processes across sites and of compositions across lineages. To circumvent these sources of bias, we developed CYANO-MLP, a machine learning algorithm that consistently and accurately phylogenetically classifies ("phyloclassifies") cyanobacterial genomes to their clade of origin based on bioinformatically predicted function-informative features in tRNA gene complements. Classification of cyanobacterial genomes with CYANO-MLP is accurate and robust to deletion of clades, unbalanced sampling, and compositional heterogeneity in input tRNA data. CYANO-MLP consistently classifies plastid genomes into a late-branching cyanobacterial sub-clade containing single-cell, starch-producing, nitrogen-fixing ecotypes, consistent with metabolic and gene transfer data. CONCLUSIONS: Phylogenomic data of cyanobacteria and plastids exhibit both site-process heterogeneities and compositional heterogeneities across lineages. These aspects of the data require careful modeling to avoid bias in phylogenomic estimation. Furthermore, we show that amino acid recoding strategies may be insufficient to mitigate bias from compositional heterogeneities. However, the combination of our novel tRNA-specific strategy with machine learning in CYANO-MLP appears robust to these sources of bias with high accuracy in phyloclassification of cyanobacterial genomes. CYANO-MLP consistently classifies plastids as late-branching Cyanobacteria, consistent with independent evidence from signature-based approaches and some previous phylogenetic studies.
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