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.
Data from: Greater pollination generalization is not associated with reduced constraints on corolla shape in Antillean plants
Contributors: Joly, Simon, Lambert, François, Alexandre, Hermine, Clavel, Julien, Léveillé-Bourret, Étienne, Clark, John L.
... Flowers show important structural variation as reproductive organs but the evolutionary forces underlying this diversity are still poorly understood. In animal-pollinated species, flower shape is strongly fashioned by selection imposed by pollinators, which is expected to vary according to guilds of effective pollinators. Using the Antillean subtribe Gesneriinae (Gesneriaceae), we tested the hypothesis that pollination specialists pollinated by one functional type of pollinator have maintained more similar corolla shapes through time due to more constant and stronger selection constraints compared to species with more generalist pollination strategies. Using geometric morphometrics and evolutionary models, we showed that the corolla of hummingbird specialists, bat specialists, and species with a mixed-pollination strategy (pollinated by hummingbirds and bats; thus a more generalist strategy) have distinct shapes and that these shapes have evolved under evolutionary constraints. However, we did not find support for greater disparity in corolla shape of more generalist species. This could be because the corolla shape of more generalist species in subtribe Gesneriinae, which has evolved multiple times, is finely adapted to be effectively pollinated by both bats and hummingbirds. These results suggest that ecological generalization is not necessarily associated with relaxed selection constraints.
Contributors: Drinan, Daniel P., Loher, Timothy, Hauser, Lorenz
... Understanding and identifying the genetic mechanisms responsible for sex-determination are important for species management, particularly in exploited fishes where sex biased harvest could have implications on population dynamics and long-term persistence. The Pacific halibut (Hippoglossus stenolepis) supports important fisheries in the North Pacific Ocean. The proportion of each sex in the annual harvest is currently estimated using growth curves, but genetic techniques may provide a more accurate method. We used restriction-site associated DNA (RAD) sequencing to identify RAD-tags that were linked to genetic sex, based on differentiation (FST) between the sexes. Identified RAD-tags were aligned to the Atlantic halibut (Hippoglossus hippoglossus) linkage map, the turbot (Scophthalmus maximus) genome, and the half-smooth tongue sole (Cynoglossus semilaevis) genome to identify genomic regions that may be involved in sex determination. In total, 56 RAD-tags (70 single nucleotide polymorphisms) were linked to sex, and three RAD-tags were identified in only females. Sex-linked loci aligned to three linkage groups in the Atlantic halibut (LG07: 7 loci, LG15: 1 locus, and LG24: 1 locus), three chromosomes in the turbot (LG12: 13 loci, LG01: 1 locus, and LG05: 1 locus), and one chromosome in the half-smooth tongue sole (ChrZ: 9 loci). Results add support to the hypothesis that Pacific halibut genetic sex is determined in a ZW system. Two sex-linked loci were further developed into sex identification assays, and their efficacy was tested on individuals that had been morphologically sexed. The accuracy of each assay on its own was 97.5% compared to morphological sex.
Data from: Prospective comparison of two models of integrating early infant male circumcision with maternal child health services in Kenya: the Mtoto Msafi Mbili Study
Contributors: Bailey, Robert C., Adera, Fredrick, Mackesy-Amiti, Mary Ellen, Adipo, Timothy, Nordstrom, Sherry K., Mehta, Supriya D., Jaoko, Walter, Langi, F. L. Fredrik G., Obiero, Walter, Obat, Edmon
... As countries scale up adult voluntary medical male circumcision (VMMC) for HIV prevention, they are looking ahead to long term sustainable strategies, including introduction of early infant male circumcision (EIMC). To address the lack of evidence regarding introduction of EIMC services in sub-Saharan African settings, we conducted a simultaneous, prospective comparison of two models of EIMC service delivery in Homa Bay County, Kenya. In one division a standard delivery package (SDP) was introduced and included health facility-based provision of EIMC services with community engagement for client referral versus in a different division a standard package plus (SDPplus) that included community-delivered EIMC services. Babies 1–60 days old were eligible for EIMC. A representative sample of mothers and fathers of baby boys at 16 health facilities was surveyed. We examined differences between mothers and fathers in the SDP and SDPplus divisions and identified factors associated with EIMC uptake. We report adjusted prevalence ratios (aPR). Of 1660 mothers interviewed, 1501 (89%) gave approval to contact the father, and 1259 fathers (84%) were interviewed. The proportion of babies circumcised was slightly greater in the SDPplus division than the SDP division (27.3% vs 23.7%), but the difference was not significant (p = 0.08). In adjusted analyses, however, the prevalence of babies being circumcised was greater in the SDPplus division (aPR = 1.23, 95% CI:1.04–1.45) and the factors associated with a baby being circumcised were the mother having received information about EIMC (during pregnancy, aPR = 4.81, 95% CI: 2.21–3.42), having discussed circumcision with the father if married or cohabiting (aPR = 5.39, 95% CI: 3.31–8.80) or being single (aPR = 5.67, 95% CI: 3.31–9.69), perceiving herself to be living with HIV (aPR = 1.39, 95% CI: 1.15–1.67), or having a post-secondary education (aPR = 1.33, 95% CI: 1.04–1.69), and the father being Muslim (aPR = 1.85, 95% CI: 1.29–2.65) or circumcised (aPR = 1.34, 95% CI: 1.13–1.59). The median age of 2117 babies circumcised was 8 days (IQR: 1–36), and the median weight was 3.6 kg (IQR: 3.2–4.4). There were 6 moderate adverse events (AEs) (0.28%); 5 severe AEs (0.24%), all involving an injury to the glans penis, requiring hospitalization and corrective surgery; and one death probably related to the procedure. There were no AEs among the 365 procedures performed outside health facilities. Information and education campaigns must reach members of the general population, especially men and fathers, who are influential to the EIMC decision. Serious AEs using the Mogen clamp are rare, but do occur and require efficient, reliable emergency back-up. Our results can assist countries considering scale-up of EIMC services for HIV prevention as their adult VMMC programs mature.
Data from: Hybrid asexuality as a primary postzygotic barrier between nascent species: on the interconnection between asexuality, hybridization and speciation
Contributors: Janko, Karel, Pačes, Jan, Wilkinson-Herbots, Hilde, Costa, Rui J., Roslein, Jan, Drozd, Pavel, Iakovenko, Nataliia, Rídl, Jakub, Hroudová, Miluše, Kočí, Jan
... Although sexual reproduction is ubiquitous throughout nature, the molecular machinery behind it has been repeatedly disrupted during evolution, leading to the emergence of asexual lineages in all eukaryotic phyla. Despite intensive research, little is known about what causes the switch from sexual reproduction to asexuality. Interspecific hybridization is one of the candidate explanations but the reasons for the apparent association between hybridization and asexuality remain unclear. In this study we combined cross-breeding experiments with population genetic and phylogenomic approaches to reveal the history of speciation and asexuality evolution in European spined loaches (Cobitis). Contemporary species readily hybridize in hybrid zones, but produce infertile males and fertile but clonally reproducing females that cannot mediate introgressions. However, our analysis of exome data indicates that intensive gene flow between species has occurred in the past. Crossings among species with various genetic distances showed that, while distantly related species produced asexual females and sterile males, closely related species produce sexually reproducing hybrids of both sexes. Our results suggest that hybridization leads to sexual hybrids at the initial stages of speciation, but as the species diverge further, the gradual accumulation of reproductive incompatibilities between species could distort their gametogenesis towards asexuality. Interestingly, comparative analysis of published data revealed that hybrid asexuality generally evolves at lower genetic divergences than hybrid sterility or inviability. Given that hybrid asexuality effectively restricts gene flow, it may establish a primary reproductive barrier earlier during diversification than other ‘classical’ forms of postzygotic incompatibilities. Hybrid asexuality may thus indirectly contribute to the speciation process.
Data from: Impact of model violations on the inference of species boundaries under the multispecies coalescent
Contributors: Barley, Anthony J., Brown, Jeremy M., Thomson, Robert C.
... The use of genetic data for identifying species-level lineages across the tree of life has received increasing attention in the field of systematics over the past decade. The multispecies coalescent model provides a framework for understanding the process of lineage divergence, and has become widely adopted for delimiting species. However, because these studies lack an explicit assessment of model fit, in many cases, the accuracy of the inferred species boundaries are unknown. This is concerning given the large amount of empirical data and theory that highlight the complexity of the speciation process. Here, we seek to fill this gap by using simulation to characterize the sensitivity of inference under the multispecies coalescent to several violations of model assumptions thought to be common in empirical data. We also assess the fit of the multispecies coalescent model to empirical data in the context of species delimitation. Our results show substantial variation in model fit across datasets. Posterior predictive tests find the poorest model performance in datasets that were hypothesized to be impacted by model violations. We also show that while the inferences assuming the multispecies coalescent are robust to minor model violations, such inferences can be biased under some biologically plausible scenarios. Taken together, these results suggest that researchers can identify individual datasets in which species delimitation under the multispecies coalescent is likely to be problematic, thereby highlighting the cases where additional lines of evidence to identify species boundaries are particularly important to collect. Our study supports a growing body of work highlighting the importance of model checking in phylogenetics, and the usefulness of tailoring tests of model fit to assess the reliability of particular inferences.
Data from: Genetic diversity and divergence in the fountain darter (Etheostoma fonticola): implications for conservation of an endangered species
Contributors: Olsen, Jeffrey B., Kinziger, Andrew P., Wenburg, John K., Lewis, Cara J., Phillips, Catherine T., Ostrand, Kenneth G.
Contributors: Berv, Jacob S., Field, Daniel J.
... Survivorship following major mass extinctions may be associated with a decrease in body size—a phenomenon called the Lilliput Effect. Body size is a strong predictor of many life history traits (LHTs), and is known to influence demography and intrinsic biological processes. Pronounced changes in organismal size throughout Earth history are therefore likely to be associated with concomitant genome-wide changes in evolutionary rates. Here, we report pronounced heterogeneity in rates of molecular evolution (varying up to ~20-fold) across a large-scale avian phylogenomic dataset, and show that nucleotide substitution rates are strongly correlated with body size and metabolic rate. We also identify potential body size reductions associated with the Cretaceous-Paleogene (K-Pg) transition, consistent with a Lilliput Effect in the wake of that mass extinction event. We posit that selection for reduced body size across the K-Pg extinction horizon may have resulted in transient increases in substitution rate along the deepest branches of the extant avian tree of life. This ‘hidden’ rate acceleration may result in both strict and relaxed molecular clocks over-estimating the age of the avian crown group through the relationship between life history and demographic parameters that scale with molecular substitution rate. If reductions in body size (and/or selection for related demographic parameters like short generation times) are a common property of lineages surviving mass extinctions, this phenomenon may help resolve persistent divergence time debates across the tree of life. Furthermore, our results suggest that selection for certain life history traits may be associated with deterministic molecular evolutionary outcomes.
Data from: Body length of bony fishes was not a selective factor during the biggest mass extinction of all time
Contributors: Puttick, Mark N., Kriwet, Jürgen, Wen, Wen, Hu, Shixue, Thomas, Gavin H., Benton, Michael J.
... The Permo-Triassic mass extinction devastated life on land and in the sea, but it is not clear why some species survived and others went extinct. One explanation is that lineage loss during mass extinctions is a random process in which luck determines which species survive. Alternatively, a phylogenetic signal in extinction may indicate a selection process operating on phenotypic traits. Large body size has often emerged as an extinction risk factor in studies of modern extinction risk, but this is not so commonly the case for mass extinctions in deep time. Here, we explore the evolution of non-teleostean Actinopterygii (bony fishes) from the Devonian to the present day, and we concentrate on the Permo-Triassic mass extinction. We apply a variety of time-scaling metrics to date the phylogeny, and show that diversity peaked in the latest Permian and declined severely during the Early Triassic. In line with previous evidence, we find the phylogenetic signal of extinction increases across the mass extinction boundary: extinction of species in the earliest Triassic is more clustered across phylogeny compared to the more randomly distributed extinction signal in the late Permian. However, body length plays no role in differential survival or extinction of taxa across the boundary. In the case of fishes, size did not determine which species survived and which went extinct, but phylogenetic signal indicates that the mass extinction was not a random field of bullets.
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.