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bioRxiv2016

A Phylogenetic Analysis of Shape Covariance Structure in the Anthropoid Skull

Phenotypic traits evolve in a coordinated manner due to developmental and functional interactions, mediated by the dynamics of natural selection; the dependence between traits arising from these three factors is captured by genetic (G) and phenotypic (P) covariance matrices. Mammalian skull development produces an intricate pattern of tissue organization and mutual signaling that integrates this structure, although the set of functions it performs is quite disparate. Therefore, the interplay between these interactions, and their relationships with the adaptive landscape may thus influence divergence in covariance structure among sister lineages. Here, we evaluate the stability of phenotypic covariance structure in skull size and shape along the diversification of Anthropoid Primates under a explicit phylogenetic framework. We estimate diversity in covariance structure, testing hypotheses concerning the phylogenetic distribution of P-matrix variation and pinpoint which traits are associated with this variation. We find that most changes occurred in the basal split between Platyrrhini and Catarrhini, and that these changes occurred within both Orbital and Basicranial trait sets, while Oral, Nasal and Vault trait sets present stable associations along the Anthropoid phylogeny. Therefore, changes in P-matrix structure among Anthropoids are restricted to trait sets whose functional significance is associated with the accommodation of the two precursor tissues that compose the skull, while the stability in the remaining regions hints at the stability of the underlying functional relationships imposed by the adaptive landscape.

evolutionary biology↗

bioRxiv2016

Taming the Late Quaternary phylogeography of the Eurasiatic wild ass through ancient and modern DNA

Taxonomic over-splitting of extinct or endangered taxa, due to an incomplete knowledge of both skeletal morphological variability and the geographical ranges of past populations, continues to confuse the link between isolated extant populations and their ancestors. This is particularly problematic with the genus Equus. To more reliably determine the evolution and phylogeographic history of the endangered Asiatic wild ass, we studied the genetic diversity and inter-relationships of both extinct and extant populations over the last 100,000 years, including samples throughout its previous range from Western Europe to Southwest and East Asia. Using 229 bp of the mitochondrial hypervariable region, an approach which allowed the inclusion of information from extremely poorly preserved ancient samples, we classify all non-African wild asses into nine clades that show a clear phylogeographic structure revealing their phylogenetic history. This study places the extinct European wild ass, E. hydruntinus, the phylogeny of which has been debated since the end of the 19th century, into its phylogenetic context within the Asiatic wild asses and reveals recent gene flow events between populations currently regarded as separate species. The phylogeographic organization of clades resulting from these efforts can be used not only to improve future taxonomic determination of a poorly characterized group of equids, but also to identify historic ranges, interbreeding events between various populations, and the impact of ancient climatic changes. In addition, appropriately placing extant relict populations into a broader phylogeographic and genetic context can better inform ongoing conservation strategies for this highly endangered species.

evolutionary biology↗

bioRxiv2016

Non-linear tradeoffs allow cooperation to evolve from Prisoner’s Dilemma to Snow Drift

The existence of cooperation, or the production of public goods, is an evolutionary problem. Cooperation is not favored because the Prisoners Dilemma (PD) game drives cooperators to extinction. We have re-analyzed this problem by using RNA viruses to motivate a model for the evolution of cooperation. Gene products are the public goods and group size is the number of virions co-infecting the same host cell. Our results show that if the tradeoff between replication and production of gene products is linear, PD is observed. However, if the tradeoff is nonlinear, the viruses evolve into separate lineages of ultra-defectors and ultra-cooperators as group size is increased. The nonlinearity was justified by the existence of real viral ultra-defectors, known as defective interfering (DI) particles, which gain a nonlinear advantage by being smaller. The evolution of ultra-defectors and ultra-cooperators creates the Snow Drift game, which promotes high-level production of public goods.

evolutionary biology↗

bioRxiv2016

The Structured Coalescent and its Approximations

Phylogenetics can be used to elucidate the movement of genes between populations of organisms, using phylogeographic methods. This has been widely done to quantify pathogen movement between different host populations, the migration history of humans, and the geographic spread of languages or the gene flow between species using the location or state of samples alongside sequence data. Phylogenies therefore offer insights into migration processes not available from classic epidemiological or occurrence data alone. Phylogeographic methods have however several known shortcomings. In particular, one of the most widely used methods treats migration the same as mutation, and therefore does not incorporate information about population demography. This may lead to severe biases in estimated migration rates for datasets where sampling is biased across populations. The structured coalescent on the other hand allows us to coherently model the migration and coalescent process, but current implementations struggle with complex datasets due to the need to infer ancestral migration histories. Thus, approximations to the structured coalescent, which integrate over all ancestral migration histories, have been developed. However, the validity and robustness of these approximations remain unclear. We present an exact numerical solution to the structured coalescent that does not require the inference of migration histories. While this solution is computationally unfeasible for large datasets, it clarifies the assumptions of previously developed approximate methods and allows us to provide an improved approximation to the structured coalescent. We have implemented these methods in BEAST2, and we show how these methods compare under different scenarios.

evolutionary biology↗

bioRxiv2016

The Tell-Tale Genome

Observable patterns of cultural variation are consistently intertwined with demic movements, cultural diffusion, and adaptation to different ecological contexts (Cavalli-Sforza and Feldman 1981; Boyd and Richerson 1985). The quantitative study of gene-culture co-evolution has focused in particular on the mechanisms responsible for change in frequency and attributes of cultural traits, on the spread of cultural information through demic and cultural diffusion, and on detecting relationships between genetic and cultural lineages. Here, for the first time, we make use of worldwide whole-genome sequences (Pagani et al. 2016) to assess the impact of demic diffusion on cultural diversity, focusing on the variability observed in folktale traditions (N=596) (Uther 2004) in Eurasia and Africa. We show that at small geographic scales (<=5000 km) there is a strong correlation between folktale and genomic distance when the effect of geography is corrected, while geographic distance has no independent effect on the distribution of folkloric narratives at the same spatial scale. This points to demic processes (i.e. population movement and replacement) as the main driver of folktale transmission at limited geographic ranges. The role of population movements becomes more apparent when regions characterized by episodes of directional expansions, such as the Neolithization of West Eurasia, are examined. Furthermore, we identify 89 individual tales which are likely to be predominantly transmitted through demic diffusion, and locate putative focal areas for a subset of them.

evolutionary biology↗

bioRxiv2016

Exploring the mutational robustness of nucleic acidsby searching genotype neighbourhoods in sequencespace

To assess the mutational robustness of nucleic acids, many genome- and protein-level studies have been performed; in these investigations, nucleic acids are treated as genetic information carriers and transferrers. However, the molecular mechanism through which mutations alter the structural, dynamic and functional properties of nucleic acids is poorly understood. Here, we performed SELEX in silico study to investigate the fitness distribution of the nucleic acid genotype neighborhood in a sequence space for L-Arm binding aptamer. Although most mutants of the L-Arm-binding aptamer failed to retain their ligand-binding ability, two novel functional genotype neighborhoods were isolated by SELEX in silico and experimentally verified to have similar binding affinity (Kd = 69.3 M and 110.7 M) as the wild-type aptamer (Kd = 114.4 M). Based on data from the current study and previous research, mutational robustness is strongly influenced by the local base environment and ligand-binding mode, whereas bases distant from the binding pocket provide potential evolutionary pathways to approach global fitness maximum. Our work provides an example of successful application of SELEX in silico to optimize an aptamer and demonstrates the strong sensitivity of mutational robustness to the site of genetic variation.

evolutionary biology↗

bioRxiv2016

Similar evolutionary trajectories for retrotransposon accumulation in mammals

The factors guiding retrotransposon insertion site preference are not well understood. Different types of retrotransposons share common replication machinery and yet occupy distinct genomic domains. Autonomous long interspersed elements accumulate in gene-poor domains and their non-autonomous short interspersed elements accumulate in gene-rich domains. To determine genomic factors that contribute to this discrepancy we analysed the distribution of retrotransposons within the framework of chromosomal domains and regulatory elements. Using comparative genomics, we identified large-scale conserved patterns of retrotransposon accumulation across several mammalian genomes. Importantly, retrotransposons that were active after our sample-species diverged accumulated in orthologous regions. This suggested a similar evolutionary interaction between retrotransposon activity and conserved genome architecture across our species. In addition, we found that retrotransposons accumulated at regulatory element boundaries in open chromatin, where accumulation of particular retrotransposon types depended on insertion size and local regulatory element density. From our results, we propose a model where density and distribution of genes and regulatory elements canalise retrotransposon accumulation. Through conservation of synteny, gene regulation and nuclear organisation, mammalian genomes with dissimilar retrotransposons follow similar evolutionary trajectories.

evolutionary biology↗

bioRxiv2016

The innate immune systems of malacostracan crustaceans exhibit both conserved and evolutionarily distinct components

Growing demands for aquatic sources of animal proteins have attracted significant investments in aquaculture research in recent years. The crustacean aquaculture industry has undergone substantial growth to accommodate a rising global demand, however such large-scale production is susceptible to pathogen-mediated destruction. It is clear that a thorough understanding of the crustacean innate immune system is imperative for future research into combating current and future pathogens of the main food crop species. Through a comparative genomics approach utilising extant data from 55 species, we describe the innate immune system of crustaceans from the Malacostraca class. We identify 7407 malacostracan genes from 39 gene families implicated in different aspects of host defence and demonstrate dynamic evolution of innate immunity components within this group. Malacostracans have achieved flexibility in recognising infectious agents through divergent evolution and expansion of pathogen recognition receptors genes. Antiviral RNAi, Toll and JAK-STAT signal transduction pathways have remained conserved within Malacostraca, although the Imd pathway appears to lack several key components. Immune effectors such as the antimicrobial peptides (AMPs) have unique evolutionary profiles, with many malacostracan AMPs not found in other arthropod groups. Lastly, we describe four putative novel immune gene families, characterised by distinct protein domains, potentially representing important evolutionary novelties of the malacostracan immune system.

evolutionary biology↗

bioRxiv2016

Recent evolution of cestode growth suppression by threespine stickleback

Parasites can be a major cause of natural selection on hosts, which consequently evolve a variety of strategies to avoid, eliminate, or tolerate infection. When ecologically similar host populations present disparate infection loads, this natural variation can reveal immunological strategies underlying adaptation to infection and population divergence. For instance, the tapeworm Schistocephalus solidus persistently infects between 0% to 80% of threespine stickleback (Gasterosteus aculeatus) in lakes on Vancouver Island. To test whether these heterogeneous infection rates are due to evolved differences in immunity, we experimentally exposed lab-reared fish from high-and low-infection populations, which are not known to differ in natural exposure risk, to controlled doses of Schistocephalus. We observed heritable between-population differences in several immune traits: fish from the naturally uninfected population initiated a stronger granulocyte response to Schistocephalus infection, and their granulocytes constitutively generated threefold more reactive oxygen species (ROS). Despite these immunological differences, Schistocephalus was equally successful at establishing initial infections in both host populations. However, the low-infection fish dramatically suppressed tapeworm growth relative to high-infection fish, and parasite size was intermediate in F1 hybrid hosts. Our results show that stickleback recently evolved heritable variation in their capacity to suppress helminth growth. Comparative data from many from natural populations indicate that growth suppression is widespread but not universal and, when present, is associated with reduced infection prevalence. Host suppression of helminth somatic growth may be an important immune strategy that aids in parasite clearance, or in mitigating the fitness costs of persistent infection.\n\nSignificanceLarge parasites remain a persistent source of morbidity and mortality in humans, domesticated animals, and wildlife. Hosts are subject to strong natural selection to eliminate or tolerate these parasite infections. Here, we document the recent evolution of a striking form of resistance by a vertebrate host (threespine stickleback) against its cestode parasite (Schistocephalus solidus). After Pleistocene glacial retreat, marine stickleback colonized freshwater lakes, encountered Schistocephalus, and evolved varying levels of resistance to it. We show that a heavily-and a rarely-infected population of stickleback have similar resistance to Schistocephalus colonization, but rarely-infected fish suppress parasite growth by orders of magnitude. These populations represent ends of a natural continuum of cestode growth suppression, which is associated with reduced infection prevalence.

evolutionary biology↗

bioRxiv2016

Non-random inversion landscapes in prokaryotic genomes are shaped by heterogeneous selection pressures

Inversions are a major contributor to structural genome evolution in prokaryotes. Here, using a novel alignment-based method, we systematically compare 1651 bacterial and 98 archaeal genomes to show that inversion landscapes are frequently biased towards (symmetric) inversions around the origin-terminus axis. However, symmetric inversion bias is not a universal feature of prokaryotic genome evolution but varies considerably across clades. At the extremes, inversion landscapes in Bacillus-Clostridium and Actinobacteria are dominated by symmetric inversions, while there is little or no systematic bias favouring symmetric rearrangements in archaea with a single origin of replication. Within clades, we find strong but clade-specific relationships between symmetric inversion bias and different features of adaptive genome architecture, including the distance of essential genes to the origin of replication and the preferential localization of genes on the leading strand. We suggest that heterogeneous selection pressures have converged to produce similar patterns of structural genome evolution across prokaryotes.

evolutionary biology↗

bioRxiv2016

Codon based co-occurrence network motifs in human mitochondria

Human mitochondrial DNA (mtDNA) generates a highly divergent pool of alleles even within species that have dispersed and expanded in size. On top of that codon position bias plays a relative role in prompting population wide sequence based variations. Codon positions are immensely studied as independent evolutionary genetic markers, however co-evolution of codon positions are still largely unexplored. Using 18,411 genome samples, we analyze nucleotide co-occurrences over mitochondrial DNA of human sub-populations covering most of the mtDNA diversity on the earth. Our codon based network motif investigation reveals that codon position is one of the critical factor to form higher order motifs. It is interesting to report a different evolution of Asian genomes than those of the rest which is divulged by motifs in non-coding regions. Most notably, we demonstrate that there are preferences of codon position co-evolution with respect to codon position sensitivity implying the selective role of evolutionary processes on fundamental formation of genetic code in terms of codon bias evolution. These network based findings not only recapitulates the established facts regarding the importance of each codon position in providing codon bias but also highlight their preferential role in resulting correlated mutations. Moreover, codon based nucleotide co-occurrence provides framework to investigate important evolutionary insights into human mitochondrial evolutionary genomics.

evolutionary biology↗

bioRxiv2016

Mobile introns shape the genetic diversity of their host genes

Self-splicing introns populate several highly conserved protein-coding genes in fungal and plant mitochondria. In fungi, many of these introns have retained their ability to spread to intron-free target sites, often assisted by intron-encoded endonucleases that initiate the homing process. Here, leveraging population genomic data from Saccharomyces cerevisiae, Schizosaccharomyces pombe, and Lachancea kluyveri, we expose non-random patterns of genetic diversity in exons that border self-splicing introns. In particular, we show that, in all three species, the density of single nucleotide polymorphisms increases as one approaches a mobile intron. Through multiple lines of evidence we rule out relaxed purifying selection as the cause of uneven nucleotide diversity. Instead, our findings implicate intron mobility as a direct driver of host gene diversity. We discuss two mechanistic scenarios that are consistent with the data: either endonuclease activity and subsequent error-prone repair have left a mutational footprint on the insertion environment of mobile introns or non-random patterns of genetic diversity are caused by exonic co-conversion, which occurs when introns spread to empty target sites via homologous recombination. Importantly, however, we show that exonic co-conversion can only explain diversity gradients near intron-exon boundaries if the conversion templates comes from outside the population. In other words, there must be pervasive and ongoing horizontal gene transfer of self-splicing introns into extant fungal populations.

evolutionary biology↗

bioRxiv2016

Phenotypic plasticity promotes recombination and gene clustering in periodic environments

The impact of changing environments on the evolution of genetic recombination is still unclear. While the Red Queen hypothesis provides a reasonable explanation for recombination, it requires coevolution with antagonistic species, such as host-parasite systems. We present a novel scenario for the evolution of recombination in changing environments: the genomic storage effect due to phenotypic plasticity. Using an analytic approximation and Monte Carlo simulations, we demonstrate that recombination evolves between a target locus that determines fitness, and a modifier locus that modulates the effects of alleles at the target. Evolution of recombination by this plasticity effect does not require antagonistic inter-specific interactions and, unlike in previous models, it occurs when only one target locus codes for a trait under selection. Furthermore, if the effects of multiple target loci are modified by the same plasticity locus, then the recombination rate among the target loci will tend to decrease, clustering the loci that influence a trait. These results provide a novel scenario for the evolution of recombination, highlighting the importance of phenotypic plasticity for recombination modification.

evolutionary biology↗

bioRxiv2016

Phenotypic plasticity can facilitate evolutionary rescue

Environmental variation is commonplace, but unpredictable. Populations that encounter a deleterious environment can sometimes avoid extinction by rapid evolutionary adaptation. Phenotypic variability, whereby a single genotype can express multiple different phenotypes, might play an important role in rescuing such populations from extinction. This type of evolutionary bet-hedging need not confer a direct benefit to a single individual, but it may increase the chance of long-term survival of a lineage. Here we develop a population-genetic model to explore how partly heritable phenotypic variability influences the probability of evolutionary rescue and the mean duration of population persistence in changing environments. We find that the probability of population persistence depends non-monotonically on the degree of phenotypic heritability between generations: some heritability can help avert extinction, but too much heritability removes any benefit of phenotypic variability. We discuss the implications of these results in the context of therapies designed to eradicate populations of pathogens or aberrant cellular lineages.

evolutionary biology↗

bioRxiv2016

The Evolution of Primate Body Size: Left-skewness, Maximum Size, and Cope’s Rule

Body size is a key physiological, ecological, and evolutionary characteristic of species. Within most major clades, body size distributions follow a right-skewed pattern where most species are relatively small while a few are orders of magnitude larger than the median size. Using a novel database of 742 extant and extinct primate species sizes over the past 66 million years, we find that primates exhibit the opposite pattern: a left-skewed distribution. We investigate the long-term evolution of this distribution, first showing that the initial size radiation is consistent with plesiadapiformes (an extinct group with an uncertain ancestral relationship to primates) being ancestral to modern primates. We calculate the strength of Copes Rule, showing an initial tendency for descendants to increase in size relative to ancestors until the trend reverses 40 million years ago. We explore when the primate size distribution becomes left-skewed and study correlations between body size patterns and climactic trends, showing that across Old and New World radiations the body size distribution initially exhibits a right-skewed pattern. Left-skewness emerged early in Old World primates in a manner consistent with a previously unidentified possible maximum body size, which may be mechanistically related to primates encephalization and complex social groups.

evolutionary biology↗

bioRxiv2016

Antisocial rewarding in structured populations

Cooperation in collective action dilemmas usually breaks down in the absence of additional incentive mechanisms. This tragedy can be escaped if cooperators have the possibility to invest in reward funds that are shared exclusively among cooperators(prosocial rewarding). Yet, the presence of defectors who do not contribute to the public good but do reward themselves(antisocial rewarding) deters cooperation in the absence of additional countermeasures. A recent simulation study suggests that spatial structure is sufficient to prevent antisocial rewarding from deterring cooperation. Here we reinvestigate this issue assuming mixed strategies and weak selection on a game-theoretic model of social interactions, which we also validate using individual-based simulations. We show that increasing reward funds facilitates the maintenance of prosocial rewarding but prevents its evolution from rare, and that spatial structure can sometimes select against the evolution of prosocial rewarding. Our results suggest that, even in spatially structured populations, additional mechanisms are required to prevent antisocial rewarding from deterring cooperation in public goods dilemmas.

evolutionary biology↗

bioRxiv2016

Conserved Non-exonic Elements: A Novel Class of Marker for Phylogenomics

Noncoding markers have a particular appeal as tools for phylogenomic analysis because, at least in vertebrates, they appear less subject to strong variation in GC content among lineages. Thus far, ultraconserved elements (UCEs) and introns have been the most widely used noncoding markers. Here we analyze and study the evolutionary properties of a new type of noncoding marker, conserved non-exonic elements (CNEEs), which consists of noncoding elements that are estimated to evolve slower than the neutral rate across a set of species. Although they often include UCEs, CNEEs are distinct from UCEs because they are not ultraconserved, and, most importantly, the core region alone is analyzed, rather than both the core and its flanking regions. Using a data set of 16 birds plus an alligator outgroup, and ~3600 - ~3800 loci per marker type, we found that although CNEEs were less variable than UCEs or introns and in some cases exhibited a slower approach to branch resolution as determined by phylogenomic subsampling, the quality of CNEE alignments was superior to those of the other markers, with fewer gaps and missing species. Phylogenetic resolution using coalescent approaches was comparable among the three marker types, with most nodes being fully and congruently resolved. Comparison of phylogenetic results across the three marker types indicated that one branch, the sister group to the passerine+falcon clade, was resolved differently and with moderate (> 70%) bootstrap support between CNEEs and UCEs or introns. Overall, CNEEs appear to be promising as phylogenomic markers, yielding phylogenetic resolution as high as for UCEs and introns but with fewer gaps, less ambiguity in alignments and with patterns of nucleotide substitution more consistent with the assumptions of commonly used methods of phylogenetic analysis.

evolutionary biology↗

bioRxiv2016

Repeated losses of PRDM9-directed recombination despite the conservation of PRDM9 across vertebrates

Studies of highly diverged species have revealed two mechanisms by which meiotic recombination is directed to the genome--through PRDM9 binding or by targeting promoter-like features--that lead to dramatically different evolutionary dynamics of hotspots. Here, we identify PRDM9 orthologs from genome and transcriptome data in 225 species. We find the complete PRDM9 ortholog across distantly related vertebrates but, despite this broad conservation, infer a minimum of six partial and three complete losses. Strikingly, taxa carrying the complete ortholog of PRDM9 are precisely those with rapid evolution of its predicted binding affinity, suggesting that all domains are necessary for directing recombination. Indeed, as we show, swordtail fish carrying only a partial but conserved ortholog share recombination properties with PRDM9 knock-outs.

evolutionary biology↗