Contributors: Ng, Julienne, Smith, Stacey D.
... Traits that have arisen multiple times yet still remain rare present a curious paradox. A number of these rare traits show a distinct tippy pattern, where they appear widely dispersed across a phylogeny, are associated with short branches, and differ between recently diverged sister species. This phylogenetic pattern has classically been attributed to the trait being an evolutionary dead end, where the trait arises due to some short‐term evolutionary advantage, but it ultimately leads species to extinction. While the higher extinction rate associated with a dead end trait could produce such a tippy pattern, a similar pattern could appear if lineages with the trait speciated slower than other lineages, or if the trait was lost more often that it was gained. In this study, we quantify the degree of tippiness of red flowers in the tomato family, Solanaceae, and investigate the macroevolutionary processes that could explain the sparse phylogenetic distribution of this trait. Using a suite of metrics, we confirm that red‐flowered lineages are significantly overdispersed across the tree and form smaller clades than expected under a null model. Next, we fit 22 alternative models using HiSSE (Hidden State Speciation and Extinction), which accommodates asymmetries in speciation, extinction and transition rates that depend on observed and unobserved (hidden) character states. Results of the model fitting indicated significant variation in diversification rates across the family, which is best explained by the inclusion of hidden states. Our best fitting model differs between the maximum clade credibility tree and when incorporating phylogenetic uncertainty, suggesting that the extreme tippiness and rarity of red Solanaceae flowers makes it difficult to distinguish among different underlying processes. However, both of the best models strongly support a bias towards the loss of red flowers. The best fitting HiSSE model when incorporating phylogenetic uncertainty lends some support to the hypothesis that lineages with red flowers exhibit reduced diversification rates due to elevated extinction rates. Future studies employing simulations or targeting population‐level processes may allow us to determine whether red flowers in Solanaceae or other angiosperms clades are rare and tippy due to a combination of processes, or asymmetrical transitions alone.
Data from: Reinstatement of the Southern Andean genus Stenodraba (Brassicaceae) based on molecular data and insights from its environmental and geographic distribution
Contributors: Salariato, Diego L., Al-Shehbaz, Ihsan A., Zuloaga, Fernando O.
... Stenodraba (Brassicaceae) included a group of eight species distributed along the Andes of South-Central Argentina and Chile. All of its species were subsequently transferred to other genera and are currently treated in Pennellia (Tribe Halimolobeae) and Weberbauera (Tribe Thelypodieae). However, the phylogeny of Stenodraba and its tribal placement were never analyzed using molecular data. The lack of such studies, as well as paucity of herbarium collections suggesting that some species are vulnerable and/or endangered, prompted us to address the molecular phylogeny of Stenodraba. For this purpose, we generated comprehensive molecular phylogenies using nuclear (ITS) and plastid (trnL-F and trnH-psbA) data, and conducted different niche comparisons in the environmental and geographic space using climate data processed both by ordination and species distribution modelling (SDM) techniques. The results demonstrated that Stenodraba belongs to the South American tribe Eudemeae and is related to the genera Aschersoniodoxa, Brayopsis, Dactylocardamum, and Eudema. Stenodraba species formed two, strongly supported clades, and although molecular data did not recover monophyly of the genus, this hypothesis was not significantly rejected. The main clades were differentiated in their climatic niches (both in the environmental and geographical spaces), and niche overlap was greater within than between clades. Systematic implications, including a key distinguishing Stenodraba from the remaining genera of Eudemeae and a synopsis of its species, are also provided.
Contributors: Faust, Ellika, Halvorsen, Kim T, Andersen, Per, Knutsen, Halvor, Carl, André
... The genetic impact of farmed fish escaping aquaculture is a highly debated issue. However, non-target species, such as cleaner fish used to remove sea lice from farmed fish, are rarely considered. Here we report that wild corkwing wrasse (Symphodus melops), which are transported long distances to be used as cleaner fish in salmon farms, escape and hybridize with local populations. Recently, increasing numbers of corkwing wrasse have been reported in Flatanger in Norway, north of its described distribution range, an area heavily relying on import of cleaner fish from Skagerrak. Using genetic markers identified with 2bRAD sequencing, we show that, although the Flatanger population largely is a result of a northwards range expansion, there is also evidence of considerable gene flow from southern populations in Skagerrak and Kattegat. Out of 40 corkwing wrasses sampled in Flatanger, we discovered two individuals with clear southern genotypes, one first generation hybrid, and twelve potential second-generation hybrids. In summary, we provide evidence that corkwing wrasse escape from fish farms and hybridize with local populations at the leading edge of an ongoing range expansion. Although the magnitude and significance of escapees warrants further investigation, these results should be taken in consideration in the use of translocated cleaner fish.
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Contributors: Blanchet, F. Guillaume, Roslin, Tomas, Kimura, Masahito T., Huotari, Tea, Kaartinen, Riikka, Gripenberg, Sofia, Tack, Ayco J. M.
... 1.Within natural communities, different taxa display different dynamics in time. Why this is the case we do not fully know. This thwarts our ability to predict changes in community structure, which is important for both the conservation of rare species in natural communities and for the prediction of pest outbreaks in agriculture. 2.Species sharing phylogeny, natural enemies and/or life history traits have been hypothesized to share similar temporal dynamics. We operationalized these concepts into testing whether feeding guild, voltinism, similarity in parasitoid community, and/or phylogenetic relatedness explained similarities in temporal dynamics among herbivorous community members. 3.Focusing on two similar data sets from different geographical regions (Finland and Japan), we used asymmetric eigenvector maps as temporal variables to characterize species- and community-level dynamics of specialist insect herbivores on oak (Quercus). We then assessed whether feeding guild, voltinism, similarity in parasitoid community, and/or phylogenetic relatedness explained similarities in temporal dynamics among taxa. 4.Species-specific temporal dynamics varied widely, ranging from directional decline or increase to more complex patterns. Phylogeny was a clear predictor of similarity in temporal dynamics at the Finnish site, whereas for the Japanese site, the data were uninformative regarding a phylogenetic imprint. Voltinism, feeding guild and parasitoid overlap explained little variation at either location. Despite the rapid temporal dynamics observed at the level of individual species, these changes did not translate into any consistent temporal changes at the community level in either Finland or Japan. 5.Overall, our findings offer no direct support for the notion that species sharing natural enemies and/or life history traits would be characterised by similar temporal dynamics, but reveal a strong imprint of phylogenetic relatedness. As this phylogenetic signal cannot be attributed to guild, voltinism or parasitoids, it will likely derive from shared microhabitat, microclimate, anatomy, physiology or behaviour. This has important implications for predicting insect outbreaks and for informing insect conservation. We hope that future studies will assess the generality of our findings across plant-feeding insect communities and beyond, and establish the more precise mechanism(s) underlying the phylogenetic imprint.
Contributors: Behrman, Emily L., Howick, Virginia M., Kapun, Martin, Staubach, Fabian, Bergland, Alan O., Petrov, Dmitri A., Lazzaro, Brian P., Schmidt, Paul S.
... Understanding the rate of evolutionary change and the genetic architecture that facilitates rapid adaptation is a current challenge in evolutionary biology. Comparative studies show that genes with immune function are among the most rapidly evolving genes across a range of taxa. Here, we use immune defence in natural populations of Drosophila melanogaster to understand the rate of evolution in natural populations and the genetics underlying rapid change. We probed the immune system using the natural pathogens Enterococcus faecalis and Providencia rettgeri to measure post-infection survival and bacterial load of wild D. melanogaster populations collected across seasonal time along a latitudinal transect along eastern North America (Massachusetts, Pennsylvania and Virginia). There are pronounced and repeatable changes in the immune response over the approximately 10 generations between spring and autumn collections, with a significant but less distinct difference observed among geographical locations. Genes with known immune function are not enriched among alleles that cycle with seasonal time, but the immune function of a subset of seasonally cycling alleles in immune genes was tested using reconstructed outbred populations. We find that flies containing seasonal alleles in Thioester-containing protein 3 (Tep3) have different functional responses to infection and that epistatic interactions among seasonal Tep3 and Drosomycin-like 6 (Dro6) alleles underlie the immune phenotypes observed in natural populations. This rapid, cyclic response to seasonal environmental pressure broadens our understanding of the complex ecological and genetic interactions determining the evolution of immune defence in natural populations.
Contributors: Teisher, Jordan K., McKain, Michael R., Schaal, Barbara A., Kellogg, Elizabeth A.
... Background and Aims: Subfamily Arundinoideae represents one of the last unsolved taxonomic mysteries in the grass family (Poaceae) due to the narrow and remote distributions of many of its 19 morphologically and ecologically heterogeneous genera. Resolving the phylogenetic relationships of these genera could have substantial implications for understanding character evolution in the grasses, for example the twisted geniculate awn – a hygroscopic awn that has been shown to be important in seed germination for some grass species. In this study, the phylogenetic positions of most arundinoid genera were determined using DNA from herbarium specimens, and their placement affects interpretation of this ecologically important trait. Methods: A phylogenetic analysis was conducted on a matrix of full-plastome sequences from 123 species in 107 genera representing all grass subfamilies, with 15 of the 19 genera in subfamily Arundinoideae. Parsimony and maximum likelihood mapping approaches were used to estimate ancestral states for presence of a geniculate lemma awn with a twisted column across Poaceae. Lastly, anatomical characters were examined for former arundinoid taxa using light microscopy and scanning electron microscopy. Key Results: Four genera traditionally included in Arundinoideae fell outside the subfamily in the plastome phylogeny, with the remaining 11 genera forming Arundinoideae sensu stricto. The twisted geniculate awn has originated independently at least five times in the PACMAD grasses, in the subfamilies Panicoideae, Danthonioideae/Chloridoideae and Arundinoideae. Morphological and anatomical characters support the new positions of the misplaced arundinoid genera in the phylogeny, but also highlight convergent and parallel evolution in the grasses. Conclusions: In placing the majority of arundinoid genera in a phylogenetic framework, our study answers one of the last remaining big questions in grass taxonomy while highlighting examples of convergent evolution in an ecologically important trait, the hygroscopic, twisted geniculate awn.
Data from: Genome-wide SNP data suggests complex ancestry of sympatric North Pacific killer whale ecotypes
Contributors: Foote, Andrew D., Morin, Phillip A.
... Three ecotypes of killer whale occur in partial sympatry in the North Pacific. Individuals assortatively mate within the same ecotype, resulting in correlated ecological and genetic differentiation. A key question is whether this pattern of evolutionary divergence is an example of incipient sympatric speciation from a single panmictic ancestral population, or whether sympatry could have resulted from multiple colonisations of the North Pacific and secondary contact between ecotypes. Here, we infer multilocus coalescent trees from >1000 nuclear single-nucleotide polymorphisms (SNPs) and find evidence of incomplete lineage sorting so that the genealogies of SNPs do not all conform to a single topology. To disentangle whether uncertainty in the phylogenetic inference of the relationships among ecotypes could also result from ancestral admixture events we reconstructed the relationship among the ecotypes as an admixture graph and estimated f4-statistics using TreeMix. The results were consistent with episodes of admixture between two of the North Pacific ecotypes and the two outgroups (populations from the Southern Ocean and the North Atlantic). Gene flow may have occurred via unsampled ‘ghost’ populations rather than directly between the populations sampled here. Our results indicate that because of ancestral admixture events and incomplete lineage sorting, a single bifurcating tree does not fully describe the relationship among these populations. The data are therefore most consistent with the genomic variation among North Pacific killer whale ecotypes resulting from multiple colonisation events, and secondary contact may have facilitated evolutionary divergence. Thus, the present-day populations of North Pacific killer whale ecotypes have a complex ancestry, confounding the tree-based inference of ancestral geography.
Data from: Para-allopatry in hybridizing fire-bellied toads (Bombina bombina and B. variegata): inference from transcriptome-wide coalescence analyses
Contributors: Nürnberger, Beate, Lohse, Konrad, Fijarczyk, Anna, Szymura, Jacek M., Blaxter, Mark L.
... Ancient origins, profound ecological divergence, and extensive hybridization make the fire-bellied toads Bombina bombina and B. variegata (Anura: Bombinatoridae) an intriguing test case of ecological speciation. Previous modeling has proposed that the narrow Bombina hybrid zones represent strong barriers to neutral introgression. We test this prediction by inferring the rate of gene exchange between pure populations on either side of the intensively studied Kraków transect. We developed a method to extract high confidence sets of orthologous genes from de novo transcriptome assemblies, fitted a range of divergence models to these data and assessed their relative support with analytic likelihood calculations. There was clear evidence for postdivergence gene flow, but, as expected, no perceptible signal of recent introgression via the nearby hybrid zone. The analysis of two additional Bombina taxa (B. v. scabra and B. orientalis) validated our parameter estimates against a larger set of prior expectations. Despite substantial cumulative introgression over millions of years, adaptive divergence of the hybridizing taxa is essentially unaffected by their lack of reproductive isolation. Extended distribution ranges also buffer them against small-scale environmental perturbations that have been shown to reverse the speciation process in other, more recent ecotypes.
Contributors: Wang, Gang, Cannon, Charles H., Chen, Jin
... Hybridization and insect pollination are widely believed to increase rates of plant diversification. The extreme diversity of figs (Ficus) and their obligate pollinators, fig wasps (Agaonidae), provides an opportunity to examine the possible role of pollinator-mediated hybridization in plant diversification. Increasing evidence suggests that pollinator sharing and hybridization occurs among fig taxa, despite relatively strict co-evolution with the pollinating wasp. Using five sympatric dioecious fig taxa and their pollinators, we examine the degree of pollinator sharing and inter-taxa gene flow. We experimentally test pollinator preference for floral volatiles, the main host recognition signal, from different figs. All five fig taxa shared pollinators with other taxa and gene flow occurred between fig taxa within and between sections. Floral volatiles of each taxon attracted more than one pollinator species. Floral volatiles were more similar between closely related figs, which experienced higher levels of pollinator sharing and inter-taxa gene flow. This study demonstrates that pollinator sharing and inter-taxa gene flow occurs among closely related sympatric dioecious fig taxa and that pollinators choose the floral volatiles of multiple fig taxa. The implications of pollinator sharing and inter-taxa gene flow on diversification, occurring even in this highly specialized obligate pollination system, requires further study.
Data from: Partial genotyping at polymorphic markers can improve heritability estimates in sibling groups
Contributors: Gauzere, J., Oddou-Muratorio, S., Gay, L., Klein, E.K.
... Accurate estimates of heritability (h²) are necessary to assess adaptive responses of populations and evolution of fitness-related traits in changing environments. For plants, h² estimates generally rely on maternal progeny designs, assuming that offspring are either half-sibs or unrelated. However, plant mating systems often depart from half-sib assumptions, this can bias h² estimates. Here, we investigate how to accurately estimate h² in non-model species through the analysis of sibling designs with a moderate genotyping effort. We performed simulations to investigate how microsatellite marker information available for only a subset of offspring can improve h² estimates based on maternal progeny designs in presence of non-random mating, inbreeding in the parental population or maternal effects. We compared the basic family method, considering or not adjustments based on average relatedness coefficients, and methods based on the animal model. The animal model was used with average relatedness information, or with hybrid relatedness information: associating one-generation pedigree and family assumptions, or associating one-generation pedigree and average relatedness coefficients. Our results highlighted that methods using marker-based relatedness coefficients performed as well as pedigree-based methods in presence of non-random mating (i.e. unequal male reproductive contributions, selfing), offering promising prospects to investigate in situ heritabilities in natural populations. In presence of maternal effects, only the use of pairwise relatednesses through pedigree information improved the accuracy of h² estimates. In that case the amount of father-related offspring in the sibling design is the most critical. Overall, we showed that the method using both one-generation pedigree and average relatedness coefficients was the most robust to various ecological scenarios.