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bioRxiv2016

Eco-evolutionary dynamics of social dilemmas

Social dilemmas are an integral part of social interactions. Cooperative actions, ranging from secreting extra-cellular products in microbial populations to donating blood in humans, are costly to the actor and hence create an incentive to shirk and avoid the costs. Nevertheless, cooperation is ubiquitous in nature. Both costs and benefits often depend non-linearly on the number and types of individuals involved-as captured by idioms such as too many cooks spoil the broth where additional contributions are discounted, or two heads are better than one where cooperators synergistically enhance the group benefit. Interaction group sizes may depend on the size of the population and hence on ecological processes. This results in feedback mechanisms between ecological and evolutionary processes, which jointly affect and determine the evolutionary trajectory. Only recently combined eco-evolutionary processes became experimentally tractable in microbial social dilemmas. Here we analyse the evolutionary dynamics of non-linear social dilemmas in settings where the population fluctuates in size and the environment changes over time. In particular, cooperation is often supported and maintained at high densities through ecological fluctuations. Moreover, we find that the combination of the two processes routinely reveals highly complex dynamics, which suggests common occurrence in nature.

Evolutionary Biology↗
bioRxiv2016

Late mitochondrial origin is pure artefact

Pittis and Gabaldon1 recently claimed that the mitochondrion came late in eukaryotic evolution, following an earlier phase of evolution in which the eukaryotic host lineage acquired genes from bacteria. Here we show that their paper has multiple fatal flaws founded in inappropriate statistical methods and analyses, in addition to erroneous interpretations.

Evolutionary Biology↗
bioRxiv2016

Specialization of a polyphenism switch gene following serial duplications in Pristionchus nematodes

Polyphenism is an extreme manifestation of developmental plasticity, requiring distinct developmental programs and the addition of a switch mechanism. Because the genetic basis of polyphenism switches has only begun to be understood, how their mechanisms arise is unclear. In the nematode Pristionchus pacificus, which has a mouthpart polyphenism specialized for alternative diets, a gene (eud-1) executing the polyphenism switch was recently identified as the product of lineage-specific duplications. Here we infer the role of gene duplications in producing a switch gene. Using reverse genetics and population genetic analyses, we examine evidence for competing scenarios of degeneration and complementation, neutral evolution, and functional specialization. Of the daughter genes, eud-1 alone has assumed switch-like regulation of the mouth polyphenism. Measurements of life-history traits in single, double, and triple sulfatase mutants did not, given modest sample sizes and a benign environment, identify alternative or complementary roles for eud-1 paralogs. Although possible roles are still unknown, selection analyses of the sister species and 104 natural isolates of P. pacificus detected purifying selection on the genes, suggesting their functionality by their fixation and evolutionary maintenance. Our approach shows the tractability of reverse genetics in a non-traditional model system to study evolution by gene duplication.

Evolutionary Biology↗
bioRxiv2016

Adaptation of mammalian myosin II sequences to body mass

The speed of muscle contraction is related to body size; muscles in larger species contract at a slower rate. We investigated the evolution of twelve myosin II isoforms to identify any adapted to increasing body mass in mammals. We identified a correlation between body mass and sequence divergence for the motor domain of three adult myosin II isoforms ({beta}, 2A, 2B) suggesting that these isoforms have adapted to increasing body mass. In contrast the non-muscle and developmental isoforms show no correlation of sequence divergence with body mass, while the sarcomeric myosin 7b, extraocular and 2X isoforms showed a divergence intermediate between these two groups. The 2B and {beta}-myosin motor domain showed the greatest rate of sequence divergence (-0.84 and -0.69 % per ten-fold increase in mass respectively). {beta}-myosin is abundant in cardiac ventricle and slow skeletal muscle. We propose that {beta}-myosin has adapted to enable slower heart beating and contraction of slow skeletal muscle as body mass increased.

Evolutionary Biology↗
bioRxiv2016

Modelling the decay of hotspot motifs in broadly neutralizing antibody lineages

Phylogenetic methods have shown great promise in understanding the development of broadly neutralizing antibody lineages (bNAbs). However, mutational process for generating these lineages - somatic hypermutation (SHM) - is biased by hotspot motifs, which violates important assumptions in most phylogenetic substitution models. Here, we develop a modified GY94-type substitution model which partially accounts for this context-dependency while preserving independence of sites in calculation. This model shows a substantially better fit to three well-characterized bNAb lineages than the standard GY94 model. We show through simulations that accounting for this can lead to reduced bias of other substitution parameters, and more accurate ancestral state reconstructions. We further explore other implications of this model; namely, that the number of hotspot motifs - and therefore likely the mutation rate in general - is expected to decay over time in individual bNAb lineages.

Evolutionary Biology↗
bioRxiv2016

Convergent evolution of genes controlling mitonuclear balance in annual fishes

Complexes of the respiratory chain are formed in a complex process where nuclearly-and mitochondrially-encoded components are assembled and inserted into the inner mitochondrial membrane. The coordination of this process is named mitonuclear balance and experimental manipulations of mitonuclear balance can increase longevity of laboratory species.\n\nHere, we investigated the pattern of positive selection in annual (i.e. short-lived)and non-annual (i.e. long-lived) African killifishes to identify a genomic substrate for evolution of annual life history (and reduced lifespan).\n\nWe identified genes under positive selection in all mitonuclear balance: mitochondrial (mt) DNA replication, transcription from mt promoters, processing and stabilization of mt RNAs, mt translation, assembly of respiratory chain complexes and electron transport chain. Signs of convergent evolution are observed in four out of five steps. This strongly indicates that these genes are preferential genetic targets for the evolution of short lifespan and annual life cycle

Evolutionary Biology↗
bioRxiv2016

The coevolutionary romance of social learning and parasitic behavior

Once an animal begins to acquire behavior by social learning, it may be seduced by parasitic parasitic, behavior that reduces the animals fitness and thereby increases its own spread. However, the animals psychology will coevolve, potentially limiting the influence and spread of parasitic behavior. I revisit prominent models of the evolution of social learning and introduce the possibility of parasitic behavior. First, I explore a courtship between primitive social learning and parasitic behavior. Parasitic behavior can spread, but selection on the host then reduces social learning and limits its importance. Both parties are frustrated. In the second part, I study a reconciliation dynamic in which social learning becomes strategic about who it partners with. In this model, parasitic behavior can become prevalent and substantially reduce host fitness. However, it may also evolve to be mutualistic and raise the mean fitness of the host organism. When this occurs, natural selection may favor psychological susceptibility to parasitic behavior. Both social learning and socially learned behavior can enjoy a happy ending.

Evolutionary Biology↗
bioRxiv2016

Information use shapes range expansion dynamics into environmental gradients

Globally, geographic distributions of species are dynamic and strongly influenced by dispersal. Vice versa, range dynamics feed back and may select for increased dispersal. This interplay almost universally happens across environmental gradients which can directly impact the fitness of organisms, but also provide individuals with information on the environmental changes. However, the organisms; ability to subsequently adjust dispersal decisions plastically has been largely ignored and the (macro)ecological consequences remain unclear. Using modeling and controlled experiments in replicated microcosm landscapes, we show that information on environmental gradients severely impacted range dynamics and inverted the spatial distribution of population densities in comparison to controls where this information was not provided. Additionally, information use prevented evolutionary changes in dispersal and an acceleration of range expansions. We demonstrate the strong impact of informed dispersal and subsequent behavioral changes on range dynamics in environmental gradients and spatial dynamics in general.

Evolutionary Biology↗
bioRxiv2016

Accounting for Uncertainty in Gene Tree Estimation: Summary-Coalescent Species Tree Inference in a Challenging Radiation of Australian Lizards

Accurate gene tree inference is an important aspect of species tree estimation in a summary-coalescent framework. Yet, in empirical studies, inferred gene trees differ in accuracy due to stochastic variation in phylogenetic signal between targeted loci. Empiricists should therefore examine the consistency of species tree inference, while accounting for the observed heterogeneity in gene tree resolution of phylogenomic datasets. Here, we assess the impact of gene tree estimation error on summary-coalescent species tree inference by screening ~2000 exonic loci based on gene tree resolution prior to phylogenetic inference. We focus on a phylogenetically challenging radiation of Australian lizards (genus Cryptoblepharus, Scincidae) and explore effects on topology and support. We identify a well-supported topology based on all loci and find that a relatively small number of high-resolution gene trees can be sufficient to converge on the same topology. Adding gene trees with decreasing resolution produced a generally consistent topology, and increased confidence for specific bipartitions that were poorly supported when using a small number of informative loci. This corroborates coalescent-based simulation studies that have highlighted the need for a large number of loci to confidently resolve challenging relationships and refutes the notion that low-resolution gene trees introduce phylogenetic noise. Further, our study also highlights the value of quantifying changes in nodal support across locus subsets of increasing size (but decreasing gene tree resolution). Such detailed analyses can reveal anomalous fluctuations in support at some nodes, suggesting the possibility of model violation. By characterizing the heterogeneity in phylogenetic signal among loci, we can account for uncertainty in gene tree estimation and assess its effect on the consistency of the species tree estimate. We suggest that the evaluation of gene tree resolution should be incorporated in the analysis of empirical phylogenomic datasets. This will ultimately increase our confidence in species tree estimation using summary-coalescent methods and enable us to exploit genomic data for phylogenetic inference.

Evolutionary Biology↗
bioRxiv2016

Why are there so many independent origins of artemisinin resistance in malaria parasites?

SummaryMultiple alleles at the kelch13 locus conferring artemisinin resistance (ART-R) are currently spreading through malaria parasite populations in Southeast Asia, providing a unique opportunity to directly observe an ongoing soft selective sweep, to investigate why resistance alleles have evolved multiple times and to determine fundamental population genetic parameters for Plasmodium. We sequenced the kelch13 gene (n=1,876), genotyped 75 flanking SNPs, and measured clearance rate (n=3,552) in parasite infections from Western Thailand (2001-2014). We describe 32 independent coding mutations: these included common mutations outside the kelch13 propeller region associated with significant reductions in clearance rate. Mutations were first observed in 2003 and rose to 90% by 2014, consistent with a selection coefficient of ~0.079. There was no change in diversity in flanking markers, but resistance allele diversity rose until 2012 and then dropped as one allele (C580Y) spread to high frequency. The rapid spread of C580Y suggests that the genomic signature may be considerably harder in the near future, and that retrospective studies may underestimate the complexity of selective sweeps. The frequency with which adaptive alleles arise is determined by the rate of mutation to generate beneficial alleles and the population size. Two factors drive this soft sweep: (1) multiple amino-acid mutations in kelch13 can confer resistance providing a large mutational target - we estimate the target size is between 87 and 163bp. (2) The population mutation parameter ({Theta}=2Ne) can be estimated from the frequency distribution of resistant alleles and is ~ 5.69, suggesting that short term effective population size is between 88 thousand and 1.2 million. This is 52 to 705-fold greater than Ne estimates based on fluctuation in allele frequencies, suggesting that we have previously underestimated the capacity for adaptive evolution in Plasmodium. Our central conclusions are that retrospective studies may underestimate the complexity of selective events, ART-R evolution is not limited by availability of mutations, and the Ne relevant for adaptation for malaria is considerably higher than previously estimated.\n\nSignificance StatementPrevious work has identified surprisingly few origins of resistance to antimalarial drugs such as chloroquine and pyrimethamine. This has lead to optimism about prospects for minimizing resistance evolution through combination therapy. We studied a longitudinal collection of malaria parasites from the Thai-Myanmar border (2001-14) to examine an ongoing selective event in which [≥]32 independent alleles associated with ART-R evolved. Three factors appear to explain the large number of origins observed: the large number of amino acid changes that result in resistance (i.e. large mutational \"target size\"), the large estimated effective population size (Ne), and the fact that we were able to document this selective event in real time, rather than retrospectively.

Evolutionary Biology↗
bioRxiv2016

When local means local: Polygenic signatures of local adaptation within whitebark pine (Pinus albicaulis Engelm.) across the Lake Tahoe Basin, USA

Patterns of local adaptation at fine spatial scales are central to understanding how evolution proceeds, and are essential to the effective management of economically and ecologically important forest tree species. Here, we employ single and multilocus analyses of genetic data (n = 116,231 SNPs) to describe signatures of fine-scale adaptation within eight whitebark pine (Pinus albicaulis Engelm.) populations across the local extent of the environmentally heterogeneous Lake Tahoe Basin, USA. We show that despite highly shared genetic variation (FST = 0.0069) there is strong evidence for adaptation to the rain shadow experienced across the eastern Sierra Nevada. Specifically, we build upon evidence from a common garden study and find that allele frequencies of loci associated with four phenotypes (mean = 236 SNPs), 18 environmental variables (mean = 99 SNPs), and those detected through genetic differentiation (n = 110 SNPs) exhibit significantly higher signals of selection (covariance of allele frequencies) than could be expected to arise, given the data. We also provide evidence that this covariance tracks environmental measures related to soil water availability through subtle allele frequency shifts across populations. Our results replicate empirical support for theoretical expectations of local adaptation for populations exhibiting strong gene flow and high selective pressures, and suggest that ongoing adaptation of many P. albicaulis populations within the Lake Tahoe Basin will not be constrained by the lack of genetic variation. Even so, some populations exhibit low levels of heritability for the traits presumed to be related to fitness. These instances could be used to prioritize management to maintain adaptive potential. Overall, we suggest that established practices regarding whitebark pine conservation be maintained, with the additional context of fine-scale adaptation.

Evolutionary Biology↗
bioRxiv2016

Sequence Entropy and the Absolute Rate of Amino Acid Substitutions

The evolution of model proteins under selection for thermodynamic stability suggests parallels between evolutionary behavior and chemical reaction kinetics. We developed a statistical mechanics theory of protein evolution by dividing amino acid interactions into site-specific and bath components, and show that substitutions between two amino acids occur when their site-specific contributions to stability are nearly identical. Fluctuating epistatic interactions drive stabilities into and out of these regions of near neutrality, with the time spent in the neutral region and thus the rate of substitution governed by physicochemical similarities between the amino acids. We derive a theoretical framework for how site-specific stabilities are determined, and demonstrate that substitution rates and the magnitude of the evolutionary Stokes shift can be predicted from biophysics and the effect of sequence entropy alone. Population genetics underlays our analysis, but population size does not determine the absolute rate of amino acid substitutions.

Evolutionary Biology↗
bioRxiv2016

Cryptic diversity and multiple origins of the widespread mayfly species group Baetis rhodani (Ephemeroptera: Baetidae) on northwestern Mediterranean islands

How the often highly endemic biodiversity of islands originated has been debated for decades and it remains a fervid research ground. Here, using mitochondrial and nuclear gene sequence analyses, we investigate the diversity, phylogenetic relationships, and evolutionary history of the mayfly Baetis gr. rhodani on the three largest north-western Mediterranean islands (Sardinia, Corsica, Elba). We identify three distinct, largely co-distributed, and deeply differentiated lineages, with divergences tentatively dated back to the Eocene-Oligocene transition. Bayesian population structure analyses reveal a lack of gene exchange between them, even at sites where they are syntopic, indicating that these lineages belong to three putative species. Their phylogenetic relationships with continental relatives, together with the dating estimates, support a role for three processes contributing to this diversity: (1) vicariance, primed by microplate disjunction and oceanic transgression; (2) dispersal from the continent; and (3) speciation within the island group. Thus, our results do not point toward a prevailing role for any of the previously invoked processes. Rather, they suggest that a variety of processes equally contributed to shape the diverse and endemic biota of this group of islands.

Evolutionary Biology↗
bioRxiv2016

Repeated range expansion and niche shift in a volcanic hotspot archipelago: radiation of Hawaiian Euphorbia (Euphorbiaceae)

Aim The taxon cycle hypothesis describes the cyclic movement of taxa during range expansion and contraction, accompanied by an evolutionary shift from open and often coastal vegetation to closed, and often inland forest vegetation in island systems. The Hawaiian Archipelago is an ideal system to test this hypothesis given the linear fashion of island formation and a relatively well-understood geological history.\n\nLocation Hawaiian Islands.\n\nMethods We sampled 153 individuals in 15 of the 16 native species of Hawaiian Euphorbia section Anisophyllum on six major Hawaiian Islands, plus 11 New World close relatives, to elucidate the biogeographic movement of this lineage along the Hawaiian island chain. We used a concatenated chloroplast DNA data set of more than eight kilobases in aligned length and applied maximum likelihood and Bayesian inference for phylogenetic reconstruction. Connectivity among islands and habitat types was estimated using BayesTraits. Age and phylogeographic patterns were co-estimated using BEAST. In addition, we used nuclear ribosomal ITS and the low-copy genes LEAFY and G3pdhC to investigate the reticulate relationships within this radiation.\n\nResults We estimate that Hawaiian Euphorbia first arrived on Kauai or Niihau ca. 5 million years ago and subsequently diverged into 16 species on all major Hawaiian Islands. During this process Euphorbia dispersed from older to younger islands in a stepping-stone fashion through open, dispersal-prone habitats. Taxa that occupy closed vegetation on Kauai and Oahu evolved in situ from open vegetation taxa of the same island. Consequently, widespread species tend to occupy habitats with open vegetation, whereas single island endemic species predominantly occur in habitats with closed canopy and are only found on the two oldest islands of Kauai and Oahu.\n\nMain conclusions The spatial and temporal patterns of dispersal and range shifts in Hawaiian Euphorbia support an intra-volcanic-archipelago version of the taxon cycle hypothesis.

Evolutionary Biology↗
bioRxiv2016

Assessing sex-specific selection against deleterious alleles: males don’t pay for sex

Selection acting on males can reduce mutation load of sexual relative to asexual populations, thus mitigating the two-fold cost of sex. This requires that it seeks and destroys the same mutations as selection acting on females, but with higher efficiency, which could happen due to sexual selection-a potent evolutionary force that in most systems predominantly affects males. We used replicate populations of red flour beetles (Tribolium castaneum) to study sex-specific selection against deleterious mutations introduced with ionizing radiation. Additionally, we employed a novel approach to quantify the relative contribution of sexual selection to the overall selection observed in males. The induced mutations were selected against in both sexes, with decreased sexual competitiveness contributing, on average, over 40% of the total decline in male fitness. However, we found no evidence for selection being stronger in males than in females; in fact, we observed a non-significant trend in the opposite direction. These results suggest that selection on males does not reduce mutation load below the level expected under the (hypothetical) scenario of asexual reproduction. Thus, we found no support for the hypothesis that sexual selection contributes to the evolutionary maintenance of sex.

Evolutionary Biology↗
bioRxiv2016

Identification of microsporidia host-exposed proteins reveals a repertoire of large paralogous gene families and rapidly evolving proteins

Pathogens use a variety of secreted and surface proteins to interact with and manipulate their hosts, but a systematic approach for identifying such proteins has been lacking. To identify these host-exposed proteins, we used spatially restricted enzymatic tagging followed by mass spectrometry analysis of C. elegans infected with two species of Nematocida microsporidia. We identified 82 microsporidia proteins inside of intestinal cells, including several pathogen proteins in the nucleus. These microsporidia proteins are enriched in targeting signals, are rapidly evolving, and belong to large, Nematocida-specific gene families. We also find that large, species-specific families are common throughout microsporidia species. Our data suggest that the use of a large number of rapidly evolving species-specific proteins represents a common strategy for these intracellular pathogens to interact with their hosts. The unbiased method described here for identifying potential pathogen effectors represents a powerful approach for the study of a broad range of pathogens.

Evolutionary Biology↗
bioRxiv2016

Within-patient HIV mutation frequencies reveal fitness costs of CpG dinucleotides, drastic amino acid changes and G→A mutations

HIV has a high mutation rate, which contributes to its ability to evolve quickly. However, we know little about the fitness costs of individual HIV mutations in vivo, their distribution and the different factors shaping the viral fitness landscape. We calculated the mean frequency of transition mutations at 870 sites of the pol gene in 160 patients, allowing us to determine the cost of these mutations. As expected, we found high costs for non-synonymous and nonsense mutations as compared to synonymous mutations. In addition, we found that non-synonymous mutations that lead to drastic amino acid changes are twice as costly as those that do not and mutations that create new CpG dinucleotides are also twice as costly as those that do not. We also found that G[->]A and C[->]T mutations are more costly than A[->]G mutations. We anticipate that our new in vivo frequency-based approach will provide insights into the fitness landscape and evolvability of not only HIV, but a variety of microbes.\n\nAuthor summaryHIVs high mutation rate allows it to evolve quickly. However, most mutations probably reduce the virus ability to replicate - they are costly to the virus. Until now, the actual cost of mutations is not well understood. We used within-patient mutation frequencies to estimate the cost of 870 HIV mutations in vivo. As expected, we found high costs for non-synonymous and nonsense mutations. In addition, we found surprisingly high costs for mutations that lead to drastic amino acid changes, mutations that create new CpG sites (possibly because they trigger the hosts immune system), and G[->]A and C[->]T mutations. Our results demonstrate the power of analyzing mutant frequencies from in vivo viral populations to study costs of mutations. A better understanding of fitness costs will help to predict the evolution of HIV.

Evolutionary Biology↗
bioRxiv2016

A systematic review of post-marital residence patterns in prehistoric hunter-gatherers

Background and RationalePost-marital residence patterns refer to where a couple lives after marriage, such as near or with husbands kin (patrilocality) or wifes kin (matrilocality). These patterns influence other aspects of social organization and behavior, and potentially reveal key parts of human nature. Since the 1860s, anthropologists have sought to characterize prehistoric hunter-gatherers post-marital residence patterns by extrapolating from modern hunter-gatherers and chimpanzees behavior. For many reasons, these extrapolations are invalid. I summarized direct evidence of residence patterns from prehistoric hunter-gatherers remains.\n\nMethodsI conducted a systematic review of strontium isotope and mitochondrial DNA (mtDNA) studies of prehistoric hunter-gatherers and extinct hominins. I also carried out a systematic review of the reliability of classifying prehistoric hunter-gatherer individuals by sex. To evaluate assumptions underlying my analyses of residence patterns, I reviewed the ethnographic literature on hunter-gatherers mortuary practices as represented in the eHRAF World Cultures database.\n\nResultsThe archaeologic sites included in my review represent every inhabited continent except Australia, and their dates span almost the last 10,000 years. In the strontium isotope studies, most adults of both sexes were local, and women were slightly more likely to be local than men. Within sites, women and men had similar mtDNA distributions. Women in neighboring, contemporaneous communities had somewhat distinct mtDNA distributions from each other, while the mtDNA distributions of men in the different communities were less distinguishable. The statistical uncertainties for most summaries are fairly large. Taken together, the results indicate the burial communities were mostly endogamous and that exogamous marriages strained toward matrilocality. The very limited research on extinct hominins residence patterns is consistent with these findings. In addition, there was only a moderate correspondence between morphologic and genetic estimates of sex in adult prehistoric hunter-gatherer individuals. When I corrected for this measurement error or relied on genetic estimates of sex only, the post-marital residence pattern results shifted in the direction of greater matrilocal tendencies. Modern hunter-gatherers burial practices were consonant with the assumptions underlying my analyses.\n\nConclusionsDirect evidence from prehistoric hunter-gatherers remains indicates very different post-marital residence patterns than those extrapolated from modern hunter-gatherers and chimpanzees behavior. In prehistoric hunter-gatherer settings, endogamy may be the outcome of humans long-term mating preferences. Endogamy may have inhibited bacterial sexually transmitted diseases in prehistory and enabled the evolution of altruism in humans.\n\nO_QD\"There is something fascinating about science. One gets such wholesale returns of conjecture out of such a trifling investment of fact.\"\n\n- Mark Twain, Life on the Mississippi, 1883\n\n\"Build up the most ingenious theories and you may be sure of one thing-that fact will defy them all.\"\n\n- Fridtjof Nansen, Farthest North, 1897\n\nC_QD

Evolutionary Biology↗