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bioRxiv2017

Transcriptome sequencing and delimitation of cryptic Oscarella species (O. carmela and O. pearsei sp. nov) from California, USA.

The homoscleromorph sponge Oscarella carmela, first described from central California, USA is shown to represent two morphologically similar but phylogenetically distant species that are co-distributed. We here describe a new species as Oscarella pearsei, sp. nov. and redescribe Oscarella carmela; the original description was based upon material from both species. Further, we correct the identification of published genomic/transcriptomic resources that were originally attributed to O. carmela, and present new Illumina-sequenced transcriptome assemblies for each of these species, and the mitochondrial genome sequence for O. pearsei sp. nov. Using SSU and LSU ribosomal DNA and the mitochondrial genome, we report the phylogenetic relationships of these species relative to other Oscarella species, and find strong support for placement of O. pearsei sp. nov. in a clade defined by the presence of spherulous cells that contain paracrystalline inclusions; O. carmela lacks this cell type and is most closely related to the Western Pacific species, O. malakhovi. Oscarella pearsei sp. nov and O. carmela can be tentatively distinguished based upon gross morphological differences such as color, surface texture and extent of mucus production, but can be more reliably identified using mitochondrial and nuclear barcode sequencing, ultrastructural characteristics of cells in the mesohyl, and the morphology of the follicle epithelium which surrounds the developing embryo in reproductively active individuals. Usually, cryptic species are very closely related to each other, but in this case and in sponges generally, cryptic species may be very distantly related because sponges can be difficult to identify based upon gross morphological characteristics.

evolutionary biology↗

bioRxiv2017

Allelic Differentiation Of Complex Trait Loci Across Human Populations

How genetic variation contributes to phenotypic variation is a central question in genetics. Association signals for a complex trait are found throughout the majority of the genome suggesting much of the genome is under some degree of genetic constraint. Here, we develop a intraspecific population genetics approach to define a measure of population structure for each single nucleotide polymorphism (SNP). Using this approach, we test for evidence of stabilizing selection at complex traits and pleiotropic loci arising from the evolutionary history of 47 complex traits and common diseases. Our approach allowed us to identify traits and regions under stabilizing selection towards both global and subpopulation optima. Strongest depletion of allelic diversity was found at disease loci, indicating stabilizing selection has acted on these phenotypes in all subpopulations. Pleiotropic loci predominantly displayed evidence of stabilizing selection, often contributed to multiple disease risks, and sometimes also affected non-disease traits such as height. Risk alleles at pleiotropic disease loci displayed a more consistent direction of effect than expected by chance suggesting that stabilizing selection acting on pleiotropic loci is amplified through multiple disease phenotypes.

evolutionary biology↗

bioRxiv2017

Demography And Mating System Shape The Genome-Wide Impact Of Purifying Selection In Arabis alpina

Plant mating systems have profound effects on levels and structuring of genetic variation, and can affect the impact of natural selection. While theory predicts that intermediate outcrossing rates may allow plants to prevent accumulation of deleterious alleles, few studies have empirically tested this prediction using genomic data. Here, we study the effect of mating system on purifying selection by conducting population genomic analyses on whole-genome resequencing data from 38 European individuals of the arctic-alpine crucifer Arabis alpina. We find that outcrossing and mixed-mating populations maintain genetic diversity at similar levels, whereas highly self-fertilizing Scandinavian A. alpina show a strong reduction in genetic diversity, most likely as a result of a postglacial colonization bottleneck. We further find evidence for accumulation of genetic load in highly self-fertilizing populations, whereas the genome-wide impact of purifying selection does not differ greatly between mixed-mating and outcrossing populations. Our results demonstrate that intermediate levels of outcrossing may allow efficient selection against harmful alleles whereas demographic effects can be important for relaxed purifying selection in highly selfing populations. Thus, both mating system and demography shape the impact of purifying selection on genomic variation in A. alpina. These results are important for an improved understanding of the evolutionary consequences of mating system variation and the maintenance of mixed-mating strategies.\n\nSignificanceIntermediate outcrossing rates are theoretically predicted to maintain effective selection against harmful alleles, but few studies have empirically tested this prediction using genomic data. We used whole-genome resequencing data from alpine rock-cress to study how genetic variation and purifying selection vary with mating system. We find that populations with intermediate outcrossing rates have similar levels of genetic diversity as outcrossing populations, and that purifying selection against harmful alleles is efficient in mixed-mating populations. In contrast, self-fertilizing populations from Scandinavia have strongly reduced genetic diversity, and accumulate harmful mutations, likely as a result of demographic effects of postglacial colonization. Our results suggest that mixed-mating populations can avoid the negative evolutionary consequences of high self-fertilization rates.

evolutionary biology↗

bioRxiv2017

Predicting The Evolutionary Consequences Of Trophy Hunting On A Quantitative Trait

Some ecologists suggest that trophy hunting (e.g. harvesting males with a desirable trait above a certain size) can lead to rapid phenotypic change, which has led to an ongoing discussion about evolutionary consequences of trophy hunting. Claims of rapid evolution come from the statistical analyses of data, with no examination of whether these results are theoretically plausible. We constructed simple quantitative genetic models to explore how a range of hunting scenarios affects the evolution of a trophy such as horn length. We show that trophy hunting does lead to trophy evolution defined as change in the mean breeding value of the trait. However, the fastest rates of phenotypic change attributable to trophy hunting via evolution that are theoretically possible under standard assumptions of quantitative genetics are 1 to 2 orders of magnitude slower than the fastest rates reported from statistical analyses. Our work suggests a re-evaluation of the likely evolutionary consequences of trophy hunting would be appropriate when setting policy. Our work does not consider the ethical or ecological consequences of trophy hunting.

evolutionary biology↗

bioRxiv2017

Multiple origin but single domestication led to domesticated Asian rice

The domestication scenario that led to Asian rice (Oryza sativa) is a contentious topic. Here, we have reanalyzed a previously published large-scale wild and domesticated rice dataset, which were also analyzed by two studies but resulted in two contrasting domestication models. We suggest the analysis of false positive selective sweep regions and phylogenetic analysis of concatenated genomic regions may have been the sources that contributed to the different results. In the end, our result indicates Asian rice originated from multiple wild progenitor subpopulations; however, de novo domestication appears to have occurred only once and the domestication alleles were transferred between rice subpopulation through introgression.

evolutionary biology↗

bioRxiv2017

Social Dilemma In The External Immune System Of The Red Flour Beetle? It Is A Matter Of Time

Sociobiology has revolutionized our understanding of interactions between organisms. Interactions may present a social dilemma where the interests of individual actors do not align with those of the group as a whole. Viewed through a sociobiological lens, nearly all interactions can be described in terms of their costs and benefits and a number of them then resemble a social dilemma. Numerous experimental systems, from bacteria to mammals, have been proposed as models for studying such dilemmas. Here we make use of the external immune system of the red flour beetle, Tribolium castaneum, to investigate how the experimental duration can affect whether the external secretion comprises a social dilemma or not. Some beetles (secretors) produce a costly quinone-rich external secretion that inhibits microbial growth in the surrounding environment, providing the secretors with direct personal benefits. However, since the antimicrobial secretion acts in the environment of the beetle it is potentially also advantageous to other beetles (non-secretors), who avoid the cost of producing the secretion. We test experimentally if the secretion qualifies as a public good. We find that in the short term, costly quinone secretion can be interpreted as a public good presenting a social dilemma where the presence of secretors increases the fitness of the group. In the long run, the benefit to the group of having more secretors vanishes and actually becomes detrimental to the group. Therefore, in such semi-natural environmental conditions, it turns out that qualifying a trait as social can be a matter of timing.

evolutionary biology↗

bioRxiv2017

Like Sugar in Milk: Reconstructing the genetic history of the Parsi population

BackgroundThe Parsis, one of the smallest religious community in the world, reside in South Asia. Previous genetic studies on them, although based on low resolution markers, reported both Iranian and Indian ancestries. To understand the population structure and demographic history of this group in more detail, we analyzed Indian and Pakistani Parsi populations using high-resolution autosomal and uniparental (Y-chromosomal and mitochondrial DNA) markers. Additionally, we also assayed 108 mitochondrial DNA markers among 21 ancient Parsi DNA samples excavated from Sanjan, in present day Gujarat, the place of their original settlement in India.\n\nResultsOur extensive analyses indicated that among present-day populations, the Parsis are genetically closest to Middle Eastern (Iranian and the Caucasus) populations rather than their South Asian neighbors. They also share the highest number of haplotypes with present-day Iranians and we estimate that the admixture of the Parsis with Indian populations occurred [~]1,200 years ago. Enriched homozygosity in the Parsi reflects their recent isolation and inbreeding. We also observed 48% South-Asian-specific mitochondrial lineages among the ancient samples, which might have resulted from the assimilation of local females during the initial settlement.\n\nConclusionsWe show that the Parsis are genetically closest to the Neolithic Iranians, followed by present-day Middle Eastern populations rather than those in South Asia and provide evidence of sex-specific admixture from South Asians to the Parsis. Our results are consistent with the historically-recorded migration of the Parsi populations to South Asia in the 7thcentury and in agreement with their assimilation into the Indian sub-continents population and cultural milieu \"like sugar in milk\". Moreover, in a wider context our results suggest a major demographic transition in West Asia due to Islamic-conquest.

evolutionary biology↗

bioRxiv2017

Host population structure and treatment frequency maintain balancing selection on drug resistance

It is a truism that antimicrobial drugs select for resistance, but explaining pathogen- and population-specific variation in patterns of resistance remains an open problem. Like other common commensals, Streptococcus pneumoniae has demonstrated persistent coexistence of drug-sensitive and drug-resistant strains. Theoretically, this outcome is unlikely. We modeled the dynamics of competing strains of S. pneumoniae to investigate the impact of transmission dynamics and treatment-induced selective pressures on the probability of stable coexistence. We find that the outcome of competition is extremely sensitive to structure in the host population, although coexistence can arise from age-assortative transmission models with age-varying rates of antibiotic use. Moreover, we find that the selective pressure from antibiotics arises not so much from the rate of antibiotic use per se but from the frequency of treatment: frequent antibiotic therapy disproportionately impacts the fitness of sensitive strains. This same phenomenon explains why serotypes with longer durations of carriage tend to be more resistant. These dynamics may apply to other potentially pathogenic, microbial commensals and highlight how population structure, which is often omitted from models, can have a large impact.

evolutionary biology↗

bioRxiv2017

Single-Virion Sequencing Of Lamivudine Treated HBV Populations Reveal Population Evolution Dynamics And Demographic History

Viral populations are complex, dynamic, and fast evolving. The evolution of groups of closely related viruses in a competitive environment is termed quasispecies. To fully understand the role that quasispecies play in viral evolution, characterizing the trajectories of viral genotypes in an evolving population is the key. In particular, long-range haplotype information for thousands of individual viruses is critical; yet generating this information is non-trivial. Popular deep sequencing methods generate relatively short reads that do not preserve linkage information, while third generation sequencing methods have higher error rates that make detection of low frequency mutations a bioinformatics challenge. Here we applied BAsE-Seq, an Illumina-based single-virion sequencing technology, to eight samples from four chronic hepatitis B (CHB) patients - once before antiviral treatment and once after viral rebound due to resistance. We obtained 248-8,796 single-virion sequences per sample, which allowed us to find evidence for both hard and soft selective sweeps. We were also able to reconstruct population demographic history that was independently verified by clinically collected data. We further verified four of the samples independently on PacBio and Illumina sequencers. Overall, we showed that single-virion sequencing yields insight into viral evolution and population dynamics in an efficient and high throughput manner. We believe that single-virion sequencing is widely applicable to the study of viral evolution in the context of drug resistance, differentiating between soft or hard selective sweeps, and the reconstruction of intra-host viral population demographic history.

evolutionary biology↗

bioRxiv2017

Bayesian Phylogenetic Analysis For Diploid And Allotetraploid Species Networks

Allopolyploid species are formed by genome doubling after hybridization between otherwise intersterile parental species. Allopolyploidy is a common speciation mechanism in land plants. Here we describe and evaluate a Bayesian approach to the phylogenetic analysis of species relationships when both ordinary speciation and allopolyploidy are present. The approach takes incomplete lineage sorting into account using the multi-species coalescent model, and extends this to deal with the extra complications due to allopolyploidy. The number of hybridizations is not assumed, which means that the number of parameters varies and a reversible-jump MCMC algorithm is needed to sample from the posterior. The main restriction is that only diploids and allotetraploids are considered. The model is implemented in the BEAST framework and is an extension of Jones et al. (2013). Simulations show that the topology of the network can be reliably inferred along with estimates of other parameters.

evolutionary biology↗

bioRxiv2017

Tunneling through time: Horizontal gene transfer constrains the timing of methanogen evolution

Microbial methanogenesis may have been a major component of Earths carbon cycle during the Archaean Eon, generating a methane greenhouse that increased global temperatures enough for a liquid hydrosphere, despite the suns lower luminosity at the time. Evaluation of potential solutions to the \"faint young sun\" hypothesis by determining the age of microbial methanogenesis was limited by ambiguous geochemical evidence, and the absence of a diagnostic fossil record. To overcome these challenges, we utilize a temporal constraint: a horizontal gene transfer (HGT) event from within archaeal methanogens to the ancestor of Cyanobacteria, one of the few microbial clades with recognized crown group fossils. Results of molecular clock analyses calibrated by this HGT-propagated constraint show methanogens diverging within Euryarchaeota no later than 3.51 Ga, with methanogenesis itself likely evolving earlier. This timing provides independent support for scenarios wherein microbial methane production was important in maintaining temperatures on the early Earth.

evolutionary biology↗

bioRxiv2017

Independent pseudogenization of CYP2J19 in penguins, owls and kiwis implicates gene in red carotenoid synthesis

Carotenoids have important roles in bird behavior, including pigmentation for sexual signaling and improving color vision via retinal oil droplets. Yellow carotenoids are diet-derived, but red carotenoids (ketocarotenoids) are typically synthesized from yellow precursors via a carotenoid ketolase. Recent research on passerines has provided evidence that a cytochrome p450 enzyme, CYP2J19, is responsible for this reaction, though it is unclear if this function is phylogenetically restricted. Here I provide evidence that CYP2J19 is the carotenoid ketolase common to Aves using the genomes of 65 birds and the retinal transcriptomes of 15 avian taxa. CYP2J19 is functionally intact and robustly transcribed in all taxa except for several species adapted to foraging in dim light conditions. Two penguins, an owl and a kiwi show evidence of genetic lesions and relaxed selection in their genomic copy of CYP2J19, and six owls show evidence of marked reduction in CYP2J19 retinal transcription compared to nine diurnal avian taxa. Notably, none of these taxa are known to use red carotenoids for sexual signaling and several species of owls and penguins represent the only birds known to completely lack red retinal oil droplets. The remaining avian taxa belong to groups known to possess red oil droplets, known or expected to deposit red carotenoids in skin and/or plumage, and/or frequently forage in bright light. The loss and reduced expression of CYP2J19 is likely an adaptation to maximize retinal sensitivity, given that oil droplets reduce the amount of light available to the retina.

evolutionary biology↗

bioRxiv2017

Escalation of Memory Length in Finite Populations

The escalation of complexity is a commonly cited benefit of coevolutionary systems, but computational simulations generally fail to demonstrate this capacity to a satisfactory degree. We draw on a macroevolutionary theory of escalation to develop a set of criteria for coevolutionary systems to exhibit escalation of strategic complexity. By expanding on a previously developed model of the evolution of memory length for cooperative strategies by Kristian Lindgren, we resolve previously observed limitations to the escalation of memory length. We present long-term coevolutionary simulations showing that larger population sizes tend to support greater escalation of complexity than smaller population sizes. Additionally, escalation is sensitive to perturbation during transitions of complexity. In whole, a long-standing counter-argument to the ubiquitous nature of coevolution is resolved, suggesting that the escalation of coevolutionary arms races can be harnessed by computational simulations.

evolutionary biology↗

bioRxiv2017

The Evolutionary Dynamics Of The Odorant Receptor Gene Family In Corbiculate Bees

Insects rely on chemical information to locate food, choose mates, and detect potential predators. It has been hypothesized that adaptive changes in the olfactory system facilitated the diversification of numerous insect lineages. For instance, evolutionary changes of Odorant Receptor (OR) genes often occur in parallel with modifications in life history strategies. Corbiculate bees display a diverse array of behaviors that are controlled through olfaction, including varying degrees of social organization, and manifold associations with floral resources. Here we investigated the molecular mechanisms driving the evolution of the OR gene family in corbiculate bees in comparison to other chemosensory gene families. Our results indicate that the genomic organization of the OR gene family has remained highly conserved for approximately 80 million years, despite exhibiting major changes in repertoire size among bee lineages. Moreover, the evolution of OR genes appears to be driven mostly by lineage-specific gene duplications in few genomic regions that harbor large numbers of OR genes. A selection analysis revealed that OR genes evolve under positive selection, with the strongest signals detected in recently duplicated copies. Our results indicate that chromosomal translocations had a minimal impact on OR evolution, and instead local molecular mechanisms appear to be main drivers of OR repertoire size. Our results provide empirical support to the longstanding hypothesis that positive selection shaped the diversification of the OR gene family. Together, our results shed new light on the molecular mechanisms underlying the evolution of olfaction in insects.

evolutionary biology↗

bioRxiv2017

On The Peopling Of The Americas: Molecular Evidence For The Paleoamerican And The Solutrean Models

Morphological and archaeological studies suggest that the Americas were first occupied by non-Mongoloids with Australo-Melanesian traits (the Paleoamerican model), which was subsequently followed by Southwest Europeans coming in along the pack ice of the North Atlantic Ocean (the Solutrean model) and by East Asians and Siberians arriving by way of the Bering Strait. Past DNA studies, however, have produced different accounts. With a better understanding of genetic diversity, we have now reinterpreted public DNA data. Consistent with our recent finding of a close relationship between South Pacific populations and Denisovans or Neanderthals who were archaic Africans with Eurasian admixtures, the [~]9500 year old Kennewick Man skeleton with Australo-Melanesian affinity from North America was about equally related to Europeans and Africans, least related to East Asians among present-day people, and most related to the [~]42000 year old Neanderthal Mezmaiskaya-2 from Adygea Russia among ancient Eurasian DNAs. The [~]12700 year old Anzick-1 of the Clovis culture was most related to the [~]18720 year old El Miron of the Magdalenian culture in Spain among ancient DNAs. Amerindian mtDNA haplotypes, unlike their Eurasian sister haplotypes, share informative SNPs with Australo-Melanesians, Africans, or Neanderthals. These results suggest a unifying account of informative findings on the settlement of the Americas.

evolutionary biology↗

bioRxiv2017

Are Global Hotspots Of Endemic Richness Shaped By Plate Tectonics?

Singular regions of the globe harbour a disproportionally large fraction of extant biodiversity. Spatial biodiversity gradients are frequently associated to extant ecological conditions using statistical models, but more rarely to paleo-environmental conditions, especially beyond the Quaternary. On one hand the role of plate tectonics in shaping the extant diversity of lineages is supported by numerous phylogenetic and fossil evidences, and on the other hand the spatial variation of biodiversity across the globe is rarely associated to geodynamic variables. In this study, we propose that plate tectonics explain the current location of hotspots of endemic richness across the globe. As an illustration, we used paleogeographies in a model, which quantifies through time and for each cell the potential dispersal across disconnected habitat patches. Rare events of dispersal across dynamic straits of unsuitable habitats allows species colonisation and that a subsequent absence of gene flow could lead to in-situ speciation. We evaluated whether this process could pinpoint the locations of hotspots of endemic richness computed from the ranges of 181,603 species across 14 taxonomic groups. The significant congruence between the regions highlighted by the model and the endemic richness provides evidences of the contribution of plate tectonics in shaping global biodiversity gradients. Places with high tectonic complexity, predominantly located at the confluence of major lithospheric plates such as the Mediterranean basin, Central America, Madagascar and South East Asia likely provided favourable circumstances for allopatric speciation and the emergence of new species across straits. While our illustration supports the role of plate tectonics, accounting for deep time geological events in spatial models of extant biodiversity is not straightforward. Future research should develop quantitative spatial models of biodiversity including the dynamic of ancient habitats.

evolutionary biology↗

bioRxiv2017

Signature Of Co-Evolution Between Defense And Vegetative Lifespan Strategies In Arabidopsis thaliana

The selective impact of pathogen epidemics on host defenses can be strong but remains transient. By contrast, life-history shifts can durably and continuously modify the balance between costs and benefits of immunity, which arbitrates the evolution of host defenses. Their impact on the evolutionary dynamics of host immunity, however, has seldom been documented. Optimal investment into immunity is expected to decrease with shortening lifespan, because a shorter life decreases the probability to encounter pathogens or enemies. Here, we document that in natural populations of Arabidopsis thaliana, the expression levels of immunity genes correlate positively with flowering time, which in annual species is a proxy for lifespan. Using a novel genetic strategy based on bulk-segregants, we partitioned flowering time-dependent from - independent immunity genes and could demonstrate that this positive co-variation can be genetically separated. It is therefore not explained by the pleiotropic action of some major regulatory genes controlling both immunity and lifespan. Moreover, we find that immunity genes containing variants reported to impact fitness in natural field conditions are among the genes whose expression co-varies most strongly with flowering time. Taken together, these analyses reveal that natural selection has likely assorted alleles promoting lower expression of immunity genes with alleles that decrease the duration of vegetative lifespan in A. thaliana and vice versa. This is the first study documenting a pattern of variation consistent with the impact that selection on flowering time is predicted to have on diversity in host immunity.

evolutionary biology↗

bioRxiv2017

Interpreting Differentiation Landscapes In The Light Of Long-Term Linked Selection

Identifying genomic regions underlying adaptation in extant lineages is key to understand the trajectories along which biodiversity evolves. However, this task is complicated by evolutionary processes that obscure and mimic footprints of positive selection. Particularly the long-term effects of linked selection remain underappreciated and difficult to account for. Based on patterns emerging from recent research on the evolution of differentiation across the speciation continuum, I illustrate how long-term linked selection affects the distribution of differentiation along genomes. I then argue that a comparative population genomics framework that exploits emergent features of long-term linked selection can help overcome shortcomings of traditional genome scans for adaptive evolution, but needs to account for the temporal dynamics of differentiation landscapes.

evolutionary biology↗