Data from: Post-glacial colonization of northern coastal habitat by bottlenose dolphins: a marine leading-edge expansion?
Contributors: Nykänen, Milaja, Kaschner, Kristin, Dabin, Willy, Brownlow, Andrew, Davison, Nicholas, Deaville, Rob, Garilao, Cristina, Kesner-Reyes, Kathleen, Gilbert, Thomas, Penrose, Rod
... Oscillations in the Earth’s temperature and the subsequent retreating and advancing of ice-sheets around the polar regions are thought to have played an important role in shaping the distribution and genetic structuring of contemporary high-latitude populations. After the Last Glacial Maximum (LGM), retreating of the ice-sheets would have enabled early colonizers to rapidly occupy suitable niches to the exclusion of other conspecifics, thereby reducing genetic diversity at the leading-edge. Bottlenose dolphins (genus Tursiops) form distinct coastal and pelagic ecotypes, with finer scale genetic structuring observed within each ecotype. We reconstruct the post-glacial colonization of the Northeast Atlantic (NEA) by bottlenose dolphins using habitat modelling and phylogenetics. The AquaMaps model hindcasted suitable habitat for the LGM in the Atlantic lower latitude waters and parts of the Mediterranean Sea. The time-calibrated phylogeny, constructed with 86 complete mitochondrial genomes including 30 generated for this study and created using a multi-species coalescent model, suggests that the expansion to the available coastal habitat in the NEA happened via founder events starting ~15,000 years ago (95% highest posterior density interval: 4,900–26,400). The founders of the two distinct coastal NEA populations comprised as few as two maternal lineages that originated from the pelagic population. The low effective population size and genetic diversity estimated for the shared ancestral coastal population subsequent to divergence from the pelagic source population are consistent with leading-edge expansion. These findings highlight the legacy of the Late Pleistocene glacial cycles on the genetic structuring and diversity of contemporary populations.
Data from: Rapid, complete reproductive isolation in two closely-related Zosterops White-eye bird species despite broadly overlapping ranges
Contributors: Cowles, Sarah A, Uy, J Albert C
... Examining what happens when two closely-related species come into secondary contact provides insight into the later stages of the speciation process. The Zosteropidae family of birds is one of the most rapidly speciating vertebrate lineages. Members of this family are highly vagile and geographically widespread, raising the question of how divergence can occur if populations can easily come into secondary contact. On the small island of Kolombangara, two closely-related non-sister species of White-eyes, Zosterops kulambangrae and Z. murphyi, are distributed along an elevational gradient and come into secondary contact at mid-elevations. We captured 134 individuals of both species along two elevational transects. Using genotyping-by-sequencing data and a mitochondrial marker, we found no evidence of past hybridization events and strong persistence of species boundaries, even though the species have only been diverging for approximately two million years. We explore potential reproductive barriers that allow the two species to coexist in sympatry, including premating isolation based on divergence in plumage and song. We also conducted a literature review to determine the time it takes to evolve complete reproductive isolation in congeneric avian species/subspecies in secondary contact (restricted to cases where congeneric taxa are parapatric or have a hybrid zone), finding our study is one of the youngest examples of complete reproductive isolation studied in a genomic context reported in birds.
Data from: Biogeography of plant root-associated fungal communities in the North-Atlantic region mirrors climatic variability
Contributors: Botnen, Synnøve Smebye, Davey, Marie L., Aas, Anders B., Carlsen, Tor, Thoen, Ella, Heegaard, Einar, Vik, Unni, Dresch, Philipp, Mundra, Sunil, Peintner, Ursula
... Aim Polar and alpine ecosystems appear to be particularly sensitive to increasing temperatures and the altered precipitation patterns linked to climate change. However, little is currently known about how these environmental drivers may affect edaphic organisms within these ecosystems. In this study, we examined communities of plant root-associated fungi (RAF) over large biogeographic scales and along climatic gradients in the North Atlantic region in order to gain insights into the potential effects of climate variability on these communities. We also investigated whether selected fungal traits were associated with particular climates. Locations Austria, Scotland, Mainland Norway, Iceland, Jan Mayen and Svalbard Taxa Root fungi associated with the ectomycorrhizal and herbaceous plant Bistorta vivipara Methods DNA metabarcoding of the ITS1 region was used to characterize the RAF of 302 whole plant root systems, which were analyzed by means of ordination methods and linear modelling. Fungal spore length, width, volume and shape, as well as mycelial exploration type of ectomycorrhizal (ECM) basidiomycetes were summarized at a community level. Results The RAF communities exhibited strong biogeographic structuring, and both compositional variation as well as fungal species richness correlated with annual temperature and precipitation. In accordance with general island biogeography theory, the least speciose RAF communities were found on Jan Mayen, a remote and small island in the North Atlantic Ocean. Fungal spores tended to be more elongated with increasing latitude. We also observed a climate effect on which mycelial exploration type was dominating among the ectomycorrhizal fungi. Main conclusions. Both geographic and environmental variables were important for shaping root associated fungal communities at a North-Atlantic scale, including the High Arctic. Fungal OTU richness followed general biogeographical patterns and decreased with decreasing size and/or increasing isolation of the host plant population. The probability of possessing more elongated spores increases with latitude, which may be explained by a selection for greater dispersal capacity among more isolated host plant populations in the Arctic.
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Data from: A genome-wide investigation of the worldwide invader Sargassum muticum shows high success albeit (almost) no genetic diversity
Contributors: Le Cam, Sabrina, Daguin-Thiébaut, Claire, Bouchemousse, Sarah, Engelen, Aschwin, Mieszkowska, Nova, Viard, Frédérique
... Twenty-years of genetic studies of marine invaders have shown that successful invaders are often characterized by native and introduced populations displaying similar levels of genetic diversity. This pattern is presumably due to high propagule pressure and repeated introductions. The opposite pattern is reported in this study of the brown seaweed, Sargassum muticum, an emblematic species for circumglobal invasions. Albeit demonstrating polymorphism in the native range, microsatellites failed to detect any genetic variation over 1269 individuals sampled from 46 locations over the Pacific-Atlantic introduction range. Single-Nucleotide Polymorphisms (SNPs) obtained from ddRAD-sequencing revealed some genetic variation, but confirmed severe founder events in both the Pacific and Atlantic introduction ranges. Our study thus exemplifies the need for extreme caution in interpreting neutral genetic diversity as a proxy for invasive potential. Our results confirm a previously hypothesized trans-oceanic secondary introduction from NE Pacific to Europe. However, the SNPs panel unexpectedly revealed two additional distinct genetic origins of introductions. Also, conversely to scenarios based on historical records, southern rather than northern NE Pacific populations could have seeded most of the European populations. Finally, the most recently introduced populations showed the lowest selfing rates, suggesting higher levels of recombination might be beneficial at the early stage of the introduction process (i.e., facilitating evolutionary novelties), whereas uniparental reproduction might be favored later in sustainably established populations (i.e., sustaining local adaptation).
Data from: Range-wide population genomics of the Mexican fruit fly: towards development of pathway analysis tools
Contributors: Dupuis, Julian R., Ruiz-Arce, Raul, Barr, Norman B., Thomas, Donald B., Geib, Scott M.
... Recurrently invading pests provide unique challenges for pest management, but also present opportunities to utilize genomics to understand invasion dynamics and inform regulatory management through pathway analysis. In the southern United States, the Mexican fruit fly Anastrepha ludens is such a pest, and its incursions into Texas and California represent major threats to the agricultural systems of those regions. We developed a draft genome assembly for A. ludens, conducted range-wide population genomics using restriction-site associated DNA sequencing, and then developed and demonstrated a panel of highly-differentiated diagnostic SNPs for source determination of intercepted flies in this system. Using 2,081 genome-wide SNPs, we identified four populations across the range of A. ludens, corresponding to western Mexico, eastern Mexico/Texas, Guatemala/Belize/Honduras, and Costa Rica/Panama, with some intergradation present between clusters, particularly in Central America. From this population genomics framework, we developed a diagnostic panel of 28 highly-differentiated SNPs that were able to recreate the genome-wide population structure in this species. We demonstrated this panel on a set of test specimens, including specimens intercepted as part of regular trapping surveillance in Texas and California, and we were able to predict populations of origin for these specimens. This methodology presents a highly applied use of genomic techniques and can be implemented in any group of recurrently invading pests.
Contributors: Hughes, Graham M., Finarelli, John A.
... The olfactory bulb (OB) ratio is the size of the olfactory bulb relative to the cerebral hemisphere, and is used to estimate the proportion of the forebrain devoted to smell. In birds, OB ratio correlates with the number of olfactory receptor (OR) genes and therefore has been used as a proxy for olfactory acuity. By coupling OB ratios with known OR gene repertoires in birds, we infer minimum repertoire sizes for extinct taxa, including non-avian dinosaurs, using phylogenetic modeling, ancestral state reconstruction and comparative genomics. We highlight a shift in the scaling of OB ratio to body size along the lineage leading to modern birds, demonstrating variable OR repertoires present in different dinosaur and crown-bird lineages, with varying factors potentially influencing sensory evolution in theropods. We investigate the ancestral sensory space available to extinct taxa, highlighting potential adaptations to ecological niches. Through combining morphological and genomic data, we show that, while genetic information for extinct taxa is forever lost, it is potentially feasible to investigate evolutionary trajectories in extinct genomes.
Data from: Detection of environmental and morphological adaptation despite high landscape genetic connectivity in a pest grasshopper (Phaulacridium vittatum)
Contributors: Yadav, Sonu, Stow, Adam J., Dudaniec, Rachael Y.
... Widespread species that exhibit both high gene flow and the capacity to occupy heterogeneous environments make excellent models for examining local selection processes along environmental gradients. Here we evaluate the influence of temperature and landscape variables on genetic connectivity and signatures of local adaptation in Phaulacridium vittatum, a widespread agricultural pest grasshopper, endemic to Australia. With sampling across a 900 km latitudinal gradient, we genotyped 185 P. vittatum from 19 sites at 11,408 single nucleotide polymorphisms (SNPs) using ddRAD sequencing. Despite high gene flow across sites (pairwise Fst = 0.0003-0.08), landscape genetic resistance modelling identified a positive non-linear effect of mean annual temperature on genetic connectivity. Urban areas and water bodies had a greater influence on genetic distance among sites than pasture, agricultural areas, and forest. Together, Fst outlier tests and Environmental Association Analysis (EAA) detected 242 unique SNPs under putative selection, with the highest numbers associated with latitude, mean annual temperature, and body size. A combination of landscape genetic connectivity analysis together with EAA identified mean annual temperature as a key driver of both neutral gene flow and environmental selection processes. Gene annotation of putatively adaptive SNPs matched with gene functions for olfaction, metabolic detoxification and ultra-violet light shielding. Our results imply that this widespread agricultural pest has the potential to spread and adapt under shifting temperature regimes and land cover change.
Data from: Outstanding intraindividual genetic diversity in fissiparous planarians (Dugesia, Platyhelminthes) with facultative sex
Contributors: Leria, Laia, Vila-Farré, Miquel, Solà, Eduard, Riutort, Marta
... Background: Predicted genetic consequences of asexuality include high intraindividual genetic diversity (i.e., the Meselson effect) and accumulation of deleterious mutations (i.e., Muller’s Ratchet), among others. These consequences have been largely studied in parthenogenetic organisms, but studies on fissiparous species are scarce. Differing from parthenogens, fissiparous organisms inherit part of the soma of the progenitor, including somatic mutations. Thus, in the long term, fissiparous reproduction may also result in genetic mosaicism, besides the presence of the Meselson effect and Muller’s Ratchet. Dugesiidae planarians show outstanding regeneration capabilities, allowing them to naturally reproduce by fission, either strictly or combined with sex (facultative). Therefore, they are an ideal model to analyze the genetic footprint of fissiparous reproduction, both when it is alternated with sex and when it is the only mode of reproduction. Results: In the present study, we generate and analyze intraindividual cloned data of a nuclear and a mitochondrial gene of sexual, fissiparous and facultative wild populations of the species Dugesia subtentaculata. We find that most individuals, independently of their reproductive strategy, are mosaics. However, the intraindividual haplotype and nucleotide diversity of fissiparous and facultative individuals is significantly higher than in sexual individuals, with no signs of Muller’s Ratchet. Finally, we also find that this high intraindividual genetic diversity of fissiparous and facultative individuals is composed by different combinations of ancestral and derived haplotypes of the species. Conclusions: The intraindividual analyses of genetic diversity point out that fissiparous reproduction leaves a very special genetic footprint in individuals, characterized by mosaicism combined with the Meselson effect (named in the present study as the mosaic Meselson effect). Interestingly, the different intraindividual combinations of ancestral and derivate genetic diversity indicate that haplotypes generated during periods of fissiparous reproduction can be also transmitted to the progeny through sexual events, resulting in offspring showing a wide range of genetic diversity and putatively allowing purifying selection to act at both intraindividual and individual level. Further investigations, using Dugesia planarians as model organisms, would be of great value to delve into this new model of genetic evolution by the combination of fission and sex.
Contributors: Chang, Ching-Ho, Chanvan, Ankita, Palladino, Jason, Wei, Xiaolu, Martins, Nuno M. C., Santinello, Bryce, Chen, Chin-Chi, Erceg, Jelena, Beliveau, Brian J., Wu, Chao-Ting
... Centromeres are essential chromosomal regions that mediate kinetochore assembly and spindle attachments during cell division. Despite their functional conservation, centromeres are amongst the most rapidly evolving genomic regions and can shape karyotype evolution and speciation across taxa. Although significant progress has been made in identifying centromere-associated proteins, the highly repetitive centromeres of metazoans have been refractory to DNA sequencing and assembly, leaving large gaps in our understanding of their functional organization and evolution. Here, we identify the sequence composition and organization of the centromeres of Drosophila melanogaster by combining long-read sequencing, chromatin immunoprecipitation for the centromeric histone CENP-A, and high-resolution chromatin fiber imaging. Contrary to previous models that heralded satellite repeats as the major functional components, we demonstrate that functional centromeres form on islands of complex DNA sequences enriched in retroelements that are flanked by large arrays of satellite repeats. Each centromere displays distinct size and arrangement of its DNA elements but is similar in composition overall. We discover that a specific retroelement, G2/Jockey-3, is the most highly enriched sequence in CENP-A chromatin and is the only element shared among all centromeres. G2/Jockey-3 is also associated with CENP-A in the sister species Drosophila simulans, revealing an unexpected conservation despite the reported turnover of centromeric satellite DNA. Our work reveals the DNA sequence identity of the active centromeres of a premier model organism and implicates retroelements as conserved features of centromeric DNA.
Data from: Birth-and-death evolution of the fatty acyl-CoA reductase (FAR) gene family and diversification of cuticular hydrocarbon synthesis in Drosophila
Contributors: Finet, Cédric, Slavik, Kailey, Pu, Jian, Carroll, Sean B., Chung, Henry
... The birth-and-death evolutionary model proposes that some members of a multigene family are phylogenetically stable and persist as a single copy over time whereas other members are phylogenetically unstable and undergo frequent duplication and loss. Functional studies suggest that stable genes are likely to encode essential functions, while rapidly evolving genes reflect phenotypic differences in traits that diverge rapidly among species. One such class of rapidly diverging traits are insect cuticular hydrocarbons (CHCs), which play dual roles in chemical communications as short-range recognition pheromones as well as protecting the insect from desiccation. Insect CHCs diverge rapidly between related species leading to ecological adaptation and/or reproductive isolation. Because the CHC and essential fatty acid biosynthetic pathways share common genes, we hypothesized that genes involved in the synthesis of CHCs would be evolutionary unstable, while those involved in fatty acid-associated essential functions would be evolutionary stable. To test this hypothesis, we investigated the evolutionary history of the fatty acyl-CoA reductases (FARs) gene family that encodes enzymes in CHC synthesis. We compiled a unique dataset of 200 FAR proteins across 12 Drosophila species. We uncovered a broad diversity in FAR content which is generated by gene duplications, subsequent gene losses, and alternative splicing. We also show that FARs expressed in oenocytes and presumably involved in CHC synthesis are more unstable than FARs from other tissues. Taken together, our study provides empirical evidence that a comparative approach investigating the birth-and-death evolution of gene families can identify candidate genes involved in rapidly diverging traits between species.