The Nicrophorus vespilloides genome and methylome, a beetle with complex social behavior
Christopher B Cunningham, Lexiang Ji, R. Axel W Wiberg, Jennifer M Shelton, Elizabeth C McKinney, Darren J Parker, Richard B Meagher, Kyle M Benowitz, Eileen M Roy-Zokan, Michael G Ritchie, Susan J Brown, Robert J Schmitz, Allen J Moore
Testing for conserved and novel mechanisms underlying phenotypic evolution requires a diversity of genomes available for comparison spanning multiple independent lineages. For example, complex social behavior in insects has been investigated primarily with eusocial lineages, nearly all of which are Hymenoptera. If conserved genomic influences on sociality do exist, we need data from a wider range of taxa that also vary in their levels of sociality. Here we present information on the genome of the subsocial beetle Nicrophorus vespilloides, a species long used to investigate evolutionary questions of complex social behavior. We used this genome to address two questions. First, does life history predict overlap in gene models more strongly than phylogenetic groupings? Second, like other insects with highly developed social behavior but unlike other beetles, does N. vespilloides have DNA methylation? We found the overlap in gene models was similar between N. vespilloides and all other insect groups regardless of life history. Unlike previous studies of beetles, we found strong evidence of DNA methylation, which allows this species to be used to address questions about the potential role of methylation in social behavior. The addition of this genome adds a coleopteran resource to answer questions about the evolution and mechanistic basis of sociality.
Stable recombination hotspots in birds
Sonal Singhal, Ellen Leffler, Keerthi Sannareddy, Isaac Turner, Oliver Venn, Daniel Hooper, Alva Strand, Qiye Li, Brian Raney, Christopher Balakrishnan, Simon Griffith, Gil McVean, Molly Przeworski
Although the DNA-binding protein PRDM9 plays a critical role in the specification of meiotic recombination hotspots in mice and apes, it appears to be absent from many vertebrate species, including birds. To learn about the determinants of fine-scale recombination rates and their evolution in natural populations lacking PRDM9, we inferred fine-scale recombination maps from population resequencing data for two bird species, the zebra finch Taeniopygia guttata, and the long-tailed finch, Poephila acuticauda, whose divergence is on par with that between human and chimpanzee. We find that both bird species have hotspots, and these are enriched near CpG islands and transcription start sites. In sharp contrast to what is seen in mice and apes, the hotspots are largely shared between the two species, with indirect evidence of conservation extending across bird species tens of millions of years diverged. These observations link the evolution of hotspots to their genetic architecture, suggesting that in the absence of PRDM9 binding specificity, accessibility of the genome to the cellular recombination machinery, particularly around functional genomic elements, both enables increased recombination and constrains its evolution.
Conflict and cooperation in eukaryogenesis: implications for the timing of endosymbiosis and the evolution of sex
Arunas L Radzvilavicius, Neil W Blackstone
The complex eukaryotic cell is a result of an ancient endosymbiosis and one of the major evolutionary transitions. The timing of key eukaryotic innovations relative to the acquisition of mitochondria remains subject to considerable debate, yet the evolutionary process itself might constrain the order of these events. Endosymbiosis entailed levels-of-selection conflicts, and mechanisms of conflict mediation had to evolve for eukaryogenesis to proceed. The initial mechanisms of conflict mediation were based on the pathways inherited from prokaryotic symbionts and led to metabolic homeostasis in the eukaryotic cell, while later mechanisms (e.g., mitochondrial gene transfer) contributed to the expansion of the eukaryotic genome. Perhaps the greatest opportunity for conflict arose with the emergence of sex involving whole-cell fusion. While early evolution of cell fusion may have affected symbiont acquisition, sex together with the competitive symbiont behaviour would have destabilised the emerging higher-level unit. Cytoplasmic mixing, on the other hand, would have been beneficial for selfish endosymbionts, capable of using their own metabolism to manipulate the life history of the host. Given the results of our mathematical modelling, we argue that sex represents a rather late proto- eukaryotic innovation, allowing for the growth of the chimeric nucleus and contributing to the successful completion of the evolutionary transition.
Morphological data is lacking for living mammals
Thomas Guillerme, Natalie Cooper
Combining living and fossil in the same analysis data is crucial for studying changes in global biodiversity through time. One method allowing to combine this data is the Total Evidence method that uses both molecular data for living species and morphological data for both living and fossil species. With this method, a good overlap of morphological data between living and fossil taxa is crucial for accurately inferring the phylogenies’ topology. Since the advent of DNA, molecular data has become easily and widely available. However, despite two centuries of morphological studies, scientists using and generating such data mainly focus on palaeontological data. Therefore, there is a gap in our knowledge of neontological morphological data even in well studied groups such as mammals. In this study, we quantify the morphological data available for living mammal taxa. We then analyse the structure of the available data by testing if it is clustered or evenly spread across the phylogeny. We found that 78% of mammalian orders have less than 25% data available at the species level. However, we found that the available is often randomly distributed among these orders apart from six of them where the data is clustered
Non-paradoxical evolutionary stability of the recombination initiation landscape in SaccharomycetesIsabel Lam, Scott Keeney
The nonrandom distribution of meiotic recombination shapes heredity and genetic diversification. A widely held view is that individual hotspots — favored sites of recombination initiation — are always ephemeral because they evolve rapidly toward extinction. An alternative view, often ignored or dismissed as implausible, predicts conservation of the positions of hotspots if they are chromosomal features under selective constraint, such as gene promoters. Here we empirically test opposite predictions of these theories by comparing genome-wide maps of meiotic recombination initiation from widely divergent species in the Saccharomyces clade. We find that the frequent overlap of hotspots with promoters is true of the species tested and, consequently, hotspot positions are well conserved. Remarkably, however, the relative strength of individual hotspots is also highly conserved, as are larger-scale features of the distribution of recombination initiation. This stability, not predicted by prior models, suggests that the particular shape of the yeast recombination landscape is adaptive, and helps in understanding evolutionary dynamics of recombination in other species.
Coalescence with background and balancing selection in systems with bi- and uniparental reproduction: contrasting partial asexuality and selfing
Aneil Agrawal, Matthew Hartfield
Uniparental reproduction in diploids, via asexual reproduction or selfing, reduces the independence with which separate loci are transmitted across generations. This is expected to increase the extent to which a neutral marker is affected by selection elsewhere in the genome. Such effects have previously been quantified in coalescent models involving selfing. Here we examine the effects of background selection and balancing selection in diploids capable of both sexual and asexual reproduction (i.e., partial asexuality). We find that the effect of background selection on reducing coalescent time (and effective population size) can be orders of magnitude greater when rates of sex are low than when sex is common. This is because asexuality enhances the effects of background selection through both a recombination effect and a segregation effect. We show that there are several reasons that the strength of background selection differs between systems with partial asexuality and those with comparable levels of uniparental reproduction via selfing. Expectations for reductions in Ne via background selection have been verified using stochastic simulations. In contrast to background selection, balancing selection increases the coalescent time for a linked neutral site. With partial asexuality, the effect of balancing selection is somewhat dependent upon the mode of selection (e.g., heterozygote advantage vs. negative frequency dependent selection) in a manner that does not apply to selfing. This is because the frequency of heterozygotes, which are required for recombination onto alternative genetic backgrounds, is more dependent on the pattern of selection with partial asexuality than with selfing.
ASTRID: Accurate Species TRees from Internode Distances
Pranjal Vachaspati, Tandy Warnow
Background: Incomplete lineage sorting (ILS), modelled by the multi-species coalescent (MSC), is known to create discordance between gene trees and species trees, and lead to inaccurate species tree estimations unless appropriate methods are used to estimate the species tree. While many statistically consistent methods have been developed to estimate the species tree in the presence of ILS, only ASTRAL-2 and NJst have been shown to have good accuracy on large datasets. Yet, NJst is generally slower and less accurate than ASTRAL-2, and cannot run on some datasets. Results: We have redesigned NJst to enable it to run on all datasets, and we have expanded its design space so that it can be used with different distance-based tree estimation methods. The resultant method, ASTRID, is statistically consistent under the MSC model, and has accuracy that is competitive with ASTRAL-2. Furthermore, ASTRID is much faster than ASTRAL-2, completing in minutes on some datasets for which ASTRAL-2 used hours. Conclusions: ASTRID is a new coalescent-based method for species tree estimation that is competitive with the best current method in terms of accuracy, while being much faster. ASTRID is available in open source form on github.
Estimating K in Genetic Mixture Models
Robert Verity, Richard Nichols
A key quantity in the analysis of structured populations is the parameter K, which describes the number of subpopulations that make up the total population. Inference of K ideally proceeds via the model evidence, which is equivalent to the likelihood of the model. However, the evidence in favour of a particular value of K cannot usually be computed exactly, and instead programs such as STRUCTURE make use of simple heuristic estimators to approximate this quantity. We show – using simulated data sets small enough that the true evidence can be computed exactly – that these simple heuristics often fail to estimate the true evidence, and that this can lead to incorrect conclusions about K. Our proposed solution is to use thermodynamic integration (TI) to estimate the model evidence. After outlining the TI methodology we demonstrate the effectiveness of this approach using a range of simulated data sets. We find that TI can be used to obtain estimates of the model evidence that are orders of magnitude more accurate and precise than those based on simple heuristics. Furthermore, estimates of K based on these values are found to be more reliable than those based on a suite of model comparison statistics. Our solution is implemented for models both with and without admixture in the software TrueK.
Adaptation to temporally fluctuating environments by the evolution of maternal effects
Snigdhadip Dey, Steve Proulx, Henrique Teotonio
Most organisms live in ever-challenging temporally fluctuating environments. Theory suggests that the evolution of anticipatory (or deterministic) maternal effects underlies adaptation to environments that regularly fluctuate every other generation because of selection for increased offspring performance. Evolution of maternal bet-hedging reproductive strategies that randomize offspring phenotypes is in turn expected to underlie adaptation to irregularly fluctuating environments. Although maternal effects are ubiquitous their adaptive significance is unknown since they can easily evolve as a correlated response to selection for increased maternal performance. Using the nematode Caenorhabditis elegans, we show the experimental evolution of maternal provisioning of offspring with glycogen, in populations facing a novel anoxia hatching environment every other generation. As expected with the evolution of deterministic maternal effects, improved embryo hatching survival under anoxia evolved at the expense of fecundity and glycogen provisioning when mothers experienced anoxia early in life. Unexpectedly, populations facing an irregularly fluctuating anoxia hatching environment failed to evolve maternal bet-hedging reproductive strategies. Instead, adaptation in these populations should have occurred through the evolution of balancing trade-offs over multiple generations, since they evolved reduced fitness over successive generations in anoxia but did not go extinct during experimental evolution. Mathematical modelling confirms our conclusion that adaptation to a wide range of patterns of environmental fluctuations hinges on the existence of deterministic maternal effects, and that they are generally much more likely to contribute to adaptation than maternal bet-hedging reproductive strategies.
Plant reproductive development is characterised by a transcriptomic evolutionary bulge
Toni I Gossmann, Dounia Saleh, Marc W Schmid, Michael A Spence, Karl Schmid
Reproductive traits in plants tend to evolve rapidly due to various causes that include plant-pollinator coevolution and pollen competition, but the genomic basis of reproductive trait evolution is still largely unknown. To characterise evolutionary patterns of genome wide gene expression in reproductive tissues and to compare them to developmental stages of the sporophyte, we analysed evolutionary conservation and genetic diversity of protein-coding genes using microarray-based transcriptome data from three plant species, Arabidopsis thaliana, rice (Oryza sativa) and soybean (Glycine max). In all three species a significant shift in gene expression occurs during gametogenesis in which genes of younger evolutionary age and higher genetic diversity contribute significantly more to the transcriptome than in other stages. We refer to this phenomenon as ‘evolutionary bulge” during plant reproductive development because it differentiates the gametophyte from the sporophyte. The extent of the bulge pattern is much stronger than the transcriptomic hourglass, which postulates that during early embryo development an increased proportion of ancient and conserved genes contribute to the total transcriptome. In the three plant species, we observed an hourglass pattern only in A. thaliana but not in rice or soybean, which suggests that unlike the evolutionary bulge of reproductive genes the transcriptomic hourglass is not a general pattern of plant embryogenesis, which is consistent with the absence of a morphologically defined phylotypic stage in plant development