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bioRxiv2017

What shapes the continuum of reproductive isolation? Lessons from Heliconius butterflies.

The process by which species evolve can be illuminated by investigating barriers that limit gene flow between taxa. Recent radiations, such as Heliconius butterflies, offer the opportunity to compare isolation between pairs of taxa at different stages of ecological, geographic and phylogenetic divergence. We carry out a comparative analysis of existing and novel data in order to quantify the strength and direction of isolating barriers within a well-studied clade of Heliconius. Our results highlight that increased divergence is associated with the accumulation of stronger and more numerous barriers to gene flow. Wing pattern is both under natural selection for Mullerian mimicry and involved in mate choice, and therefore underlies several isolating barriers. However, pairs which share a similar wing pattern, also display strong reproductive isolation mediated by traits other than wing pattern. This suggests that, while wing pattern is a key factor for early stages of divergence, it is not essential at a higher level. Additional factors including habitat isolation, hybrid sterility and chemically-mediated mate choice are associated with complete speciation. Therefore, although most previous work has emphasised the role of wing pattern, our comparative results highlight that speciation is a multidimensional process, whose completion is stabilized by many factors.

evolutionary biology↗

bioRxiv2017

Chromosome Number of the Monarch Butterfly, Danaus plexippus (Linnaeus 1758) and the Danainae

The monarch butterfly, Danaus plexippus (Linnaeus 1758) is a charismatic butterfly known for its multi-generational migration in Eastern North America, and is emerging as an important system in the study of evolutionary genetics. Assigning genes or genetic elements to chromosomes is an important step when considering how genomes evolved. The monarch butterfly has a reported haploid chromosome number of 30. The specimens that this count is based on are from Madras, India where D. plexippus does not occur. As a consequence the reported haplotype for the D. plexippus is incorrect. A literature review revealed that the specimens this count was based on were most likely Danaus genutia (Cramer 1779), which Linnaeus and others conflated with D. plexippus. In a 1954 Opinion (#282) the International Code of Zoological Nomenclature decided that the name D. genutia refers to specimens originating from the Orient and D. plexippus to those from North America. To clarify the haplotype number of D. plexippus from North America I conducted chromosome squashes of male 5th instar larvae. All specimens examined had a haploid chromosome count of n = 28. Following these new data, I then reconstructed the evolution of haplotypes throughout the Danainae subfamily to provide a testable hypothesis on the evolution of chromosome number for this group.

evolutionary biology↗

bioRxiv2017

Functional Bias and Demographic History Obscure Patterns of Selection among Single-Copy Genes in a Fungal Species Complex

Many different evolutionary processes may be responsible for explaining natural variation within genomes, some of which include natural selection at the molecular level and changes in population size. Fungi are highly adaptable organisms, and their relatively small genomes and short generation times make them pliable for evolutionary genomic studies. However, adaptation in wild populations has been relatively less documented compared to experimental or clinical studies. Here, we analyzed DNA sequences from 502 putative single-copy orthologous genes in 63 samples that represent seven recently diverged North American Amanita (jacksonii-complex) lineages. For each gene and each species, we measured the genealogical sorting index (gsi) and infinite-site-based summary statistics, such as [Formula], [Formula] and DTaj in coding and intron regions. MKT-based approaches and likelihood-ratio-test Kn/Ks models were used to measure natural selection in all coding sequences. Multi-locus (Extended) Bayesian Skyline Plots (eBSP) were used to model intraspecific demographic changes through time based on unlinked, putative neutral regions (introns). Most genes show evidence of long-term purifying selection, likely reflecting a functional bias implicit in single-copy genes. We find that two species have strongly negatively skewed Tajimas D, while three other have a positive skew, corresponding well with patterns of demographic expansion and contraction. Standard MKT analyses resulted in a high incidence of near-zero with a tendency towards negative values. In contrast, estimates based on the distribution of fitness effects (DFE), which accounts for demographic effects and slightly deleterious mutations, suggest a higher proportion of sites fixed by positive selection. The difference was more notorious in species with expansion signatures or with historically low population sizes, evidencing the concealing effects of specific demographic histories. Finally, we attempt to mitigate Gene Ontology term overrepresentation, highlighting the potential adaptive or ecological roles of some genes under positive selection.

evolutionary biology↗

bioRxiv2017

Genomic contingencies and beak shape variation in a hybrid species

Hybridization is increasingly recognized as a potent evolutionary force. Though additive genetic variation and novel combinations of parental genes theoretically increase the potential for hybrid species to adapt, few empirical studies have investigated the adaptive potential within a hybrid species. Here, we investigate factors promoting phenotypic divergence using genomically diverged island populations of the homoploid hybrid Italian sparrow Passer italiae from Crete, Corsica, and Sicily. We address whether genomic contingencies, adaptation to climate or diet best explain divergence in beak morphology. Populations vary significantly in beak morphology, both between and within islands of origin. Temperature seasonality best explains population divergence in beak size. Interestingly, beak shape along all significant dimensions of variation was best explained by annual precipitation, genomic composition and their interaction, suggesting a role for contingencies. Moreover, beak shape similarity to a parent species correlates with proportion of the genome inherited from that species, consistent with the presence of contingencies. In conclusion, adaptation to local conditions and genomic contingencies arising from putatively independent hybridization events jointly explain beak morphology in the Italian sparrow. Hence, hybridization may induce contingencies and restrict evolution in certain directions dependent on the genetic background.

evolutionary biology↗

bioRxiv2017

Variation and constraints in hybrid genome formation

Recent genomic investigations have revealed hybridization to be an important source of variation, the working material of natural selection1,2. Hybridization can spur adaptive radiations3, transfer adaptive variation across species boundaries4, and generate species with novel niches5. Yet, the limits to viable hybrid genome formation are poorly understood. Here we investigated to what extent hybrid genomes are free to evolve or whether they are restricted to a specific combination of parental alleles by sequencing the genomes of four isolated island populations of the homoploid hybrid Italian sparrow Passer italiae6,7. Based on 61 Italian sparrow genomes from Crete, Corsica, Sicily and Malta, and 10 genomes of each of the parent species P. domesticus and P. hispaniolensis, we report that a variety of novel and fully functional hybrid genomic combinations have arisen on the different islands, with differentiation in candidate genes for beak shape and plumage colour. There are limits to successful genome fusion, however, as certain genomic regions are invariably inherited from the same parent species. These regions are overrepresented on the Z-chromosome and harbour candidate incompatibility loci, including DNA-repair and mito-nuclear genes; loci that may drive the general reduction of introgression on sex chromosomes8. Our findings demonstrate that hybridization is a potent process for generating novel variation, but variation is limited by DNA-repair and mito-nuclear genes, which play an important role in reproductive isolation and thus contribute to speciation.

evolutionary biology↗

bioRxiv2017

Variability in fitness effects and the limitations of lineage selection

Evolutionary biologists commonly assess the evolutionary advantage of an allele based on its effects on the lifetime survival and reproduction of individuals. However, alleles affecting traits like sex, evolvability, and cooperation can cause fitness effects that depend heavily on differences in the environmental, genetic, and social context of individuals carrying the allele. This variability makes it difficult to summarize the evolutionary fate of an allele based solely on its effects on any one individual. In this review we show how attempts to average over variability in the fitness effects of an allele can sometimes cause misleading results. We then describe a number of intriguing new evolutionary phenomena that have emerged in studies that explicitly model the fate of alleles that influence long-term lineage dynamics. We conclude with prospects for generalizations of population genetics theory and discuss how this theory might be applied to the evolution of infectious diseases.

evolutionary biology↗

bioRxiv2017

VICTOR: Genome-based Phylogeny and Classification of Prokaryotic Viruses

Bacterial and archaeal viruses (\"phages\") play an enormous role in global life cycles and have recently regained importance as therapeutic agents to fight serious infections by multi-resistant bacterial strains. Nevertheless, taxonomic classification of phages is up to now only insufficiently informed by genome sequencing. Despite thousands of publicly available phage genomes, it still needs to be investigated how this wealth of information can be used for the fast, universal and accurate classification of phages. The Genome BLAST Distance Phylogeny (GBDP) approach is a truly whole-genome method currently used for in silico DNA: DNA hybridization and phylogenetic inference from prokaryotic genomes. Based on the principles of phylogenetic systematics, we here established GBDP for phage phylogeny and classification, using the common subset of genome-sequenced and officially classified phages. Trees inferred with the best GBDP variants showed only few deviations from the official phage classification, which were uniformly due to incorrectly annotated GenBank entries. Except for low resolution at the family level, the majority of taxa was well supported as monophyletic. Clustering genome sequences with distance thresholds optimized for the agreement with the classification turned out to be phylogenetically reasonable. Accordingly modifying genera and species is taxonomically optional but would yield more uniform sequence divergence as well as stronger branch support. Analysing an expanded data set containing > 4000 phage genomes from public databases allowed for extrapolating regarding the number, composition and host specificity of future phage taxa. The selected methods are implemented in an easy-to-use web service \"VICTOR\" freely available at http://ggdc.dsmz.de/victor.php.

evolutionary biology↗

bioRxiv2017

Darker eggs resist more to desiccation: the case of melanin in Aedes, Anopheles and Culex mosquito vectors

Mosquito vectors lay their eggs in the aquatic milieu. During early embryogenesis water passes freely through the transparent eggshell, composed of exochorion and endochorion. Within two hours the endochorion darkens via melanization but even so eggs shrink and perish if removed from moisture. However, during mid-embryogenesis, cells of the extraembryonic serosa secretes the serosal cuticle, localized right below the endochorion, which greatly reduces water flow and allows the egg to survive outside the water. The degree of egg resistance to desiccation (ERD) at late embryogenesis varies among different species: Aedes aegypti, Anopheles aquasalis and Culex quinquefasciatus eggs can survive in a dry environment for [≥] 72, 24 and 5 hours, respectively. In some adult insects, darker-body individuals show greater resistance to desiccation than lighter ones. We asked if melanization enhances serosal cuticle-dependent ERD. Species with higher ERD at late embryogenesis exhibit more melanized eggshells. The melanization-ERD hypothesis was confirmed employing two Anopheles quadrimaculatus strains, the wild type and the mutant GORO, with a dark-brown and a golden eggshell, respectively. In all cases, serosal cuticle formation is fundamental for the establishment of an efficient ERD but egg viability outside the water is much higher in mosquitoes with darker eggshells than in those with lighter ones. The finding that pigmentation influences egg water balance is relevant to understand the evolutionary history of insect coloration. Since eggshell and adult cuticle pigmentation ensure insect survivorship in some cases, they should be considered regarding species fitness and novel approaches for vector or pest insects control.

evolutionary biology↗

bioRxiv2017

Molecular evidence for the early evolution of photosynthetic water oxidation

Photosystem II is a photochemical reaction center that catalyzes the light-driven oxidation of water to molecular oxygen. Water oxidation is the distinctive photochemical reaction that permitted the evolution of oxygenic photosynthesis and the eventual rise of Eukaryotes. At what point during the history of life an ancestral photosystem evolved the capacity to oxidize water still remains unknown. Here we study the evolution of the core reaction center proteins of Photosystem II using sequence and structural comparisons in combination with Bayesian relaxed molecular clocks. Our results indicate that a homodimeric photosystem with sufficient oxidizing power to split water had already appeared in the early Archean about a billion years before the most recent common ancestor of all described Cyanobacteria capable of oxygenic photosynthesis, and well before the diversification of some of the known groups of anoxygenic photosynthetic bacteria. Based on a structural and functional rationale we hypothesize that this early Archean photosystem was capable of water oxidation and had already evolved some level of protection against the formation of reactive oxygen species, which would place primordial forms of oxygenic photosynthesis at a very early stage in the evolutionary history of life.

evolutionary biology↗

bioRxiv2017

Niche construction in evolutionary theory: the construction of an academic niche?

In recent years, fairly far-reaching claims have been repeatedly made about how niche construction, the modification by organisms of their environment, and that of other organisms, represents a vastly neglected phenomenon in ecological and evolutionary thought. The proponents of this view claim that the niche construction perspective greatly expands the scope of standard evolutionary theory and that niche construction deserves to be treated as a significant evolutionary process in its own right, almost at par with natural selection. Claims have also been advanced about how niche construction theory represents a substantial extension to, and re-orientation of, standard evolutionary theory, which is criticized as being narrowly gene-centric and ignoring the rich complexity and reciprocity of organism-environment interactions. We examine these claims in some detail and show that they do not stand up to scrutiny. We suggest that the manner in which niche construction theory is sought to be pushed in the literature is better viewed as an exercise in academic niche construction whereby, through incessant repetition of largely untenable claims, and the deployment of rhetorically appealing but logically dubious analogies, a receptive climate for a certain sub-discipline is sought to be manufactured within the scientific community. We see this as an unfortunate, but perhaps inevitable, nascent post-truth tendency within science.

evolutionary biology↗

bioRxiv2017

The monoplastidic bottleneck in algae and plant evolution

Plant and algae plastids evolved from the endosymbiotic integration of a cyanobacterium by a heterotrophic eukaryote. A consequence of their ancestry is that new plastids can only emerge through fission and vital to organelle and host co-evolution was the early synchronization of bacterial division with the hosts eukaryotic cell cycle. Most of the sampled algae, including multicellular macroalgae, house a single plastid per cell -- or nucleus in case of coenocytic cells -- and basal branching relatives of polyplastidic lineages are all monoplastidic. The latter is also true regarding embryophytes, as some non-vascular plants are monoplastidic at least at some stage of their life cycle. Here we synthesize recent advances regarding plastid division and associated proteins, including those of the peptidoglycan wall biosynthesis, across the diversity of phototrophic eukaryotes. Through the comparison of the phenotype of 131 species harbouring plastids of primary or secondary origin, we uncover that one prerequisite for an algae or plant to house multiple plastids per nucleus appears the loss of the genes MinD and MinE from the plastid genome. Housing a single plastid whose division is coupled to host cytokinesis appears a prerequisite of plastid emergence; escaping that monoplastidic bottleneck succeeded rarely and appears tied to evolving a complex morphology. Considering how little we know about the mechanisms that guarantee proper organelle (and genome) inheritance raises the peculiar possibility that a quality control checkpoint of plastid transmission remains to be explored and which is tied to understanding the monoplastidic bottleneck.

evolutionary biology↗

bioRxiv2017

Complete mitochondrial genome of golden silk producer Antheraea assamensis and its comparative analysis with other lepidopteran insects

Muga (Antheraea assamensis) is an economically important silkmoth endemic to North-eastern part of India and is the producer of the strongest known commercial silk. However, there is a scarcity of -omics data for understanding the organism at a molecular level. Our present study decodes the complete mitochondrial genome (mitogenome) of A. assamensis and presents comparative analysis with other lepidopterans. Mitogenome is a 15,272 bp long AT rich (~80.2%) molecule containing 37 genes (13 PCGs, 22 tRNAs, 2 rRNAs) and a 328 bp long control region. The overall mitogenome arrangement was similar to the other lepidopterans. Two PCGs cox1 and cox2 were found to have CGA and GTG as start codons respectively like some lepidopterans. Typical clover-leaf shaped secondary structures of tRNAs were found with a few exceptions such as unstable DHU and T{Psi}C loop in tRNASer1 and tRNATyr; significant number of mismatches (35) spread over 19 tRNAs. The control region contained a six bp deletion atypical of other Antheraea species. Phylogenetic position was consistent with the traditional taxonomic classification of Saturniidae. The complete annotated mitogenome is available in GenBank (Accession No. KU379695). To the best of our knowledge, this is the first report on complete mitogenome of A. assamensis.

evolutionary biology↗

bioRxiv2017

Evolution and manipulation of vector host choice

The transmission of many animal and plant diseases relies on the behavior of arthropod vectors. In particular, the choice to feed on either infected or uninfected hosts can dramatically affect the epidemiology of vector-borne diseases. I develop an epidemiological model to explore the impact of host choice behavior on the dynamics of these diseases and to examine selection acting on vector behavior, but also on pathogen manipulation of this behavior. This model identifies multiple evolutionary conflicts over the control of this behavior and generates testable predictions under different scenarios. In general, the vector should evolve the ability to avoid infected hosts. However, if the vector behavior is under the control of the pathogen, uninfected vectors should prefer infected hosts while infected vectors should seek uninfected hosts. But some mechanistic constraints on pathogen manipulation ability may alter these predictions. These theoretical results are discussed in the light of observed behavioral patterns obtained on a diverse range of vector-borne diseases. These patterns confirm that several pathogens have evolved conditional behavioral manipulation strategies of their vector species. Other pathogens, however, seem unable to evolve such complex conditional strategies. Contrasting the behavior of infected and uninfected vectors may thus help reveal mechanistic constraints acting on the evolution of the manipulation of vector behavior.

evolutionary biology↗

bioRxiv2017

HIV population-level adaptation can rapidly diminish the impact of a partially effective vaccine

Development of an HIV vaccine is essential to ending the HIV/AIDS pandemic. However, vaccines can result in the emergence and spread of vaccine-resistant strains. Indeed, analyses of breakthrough infections in the HIV vaccine trial RV144 identified HIV genotypes with differential rates of transmission in vaccine and placebo recipients. We hypothesized that, for HIV vaccination programs based on partially effective vaccines similar to RV144, HIV adaptation will diminish the expected vaccine impact. Using two HIV epidemic models, we simulated large-scale vaccination programs and, critically, included HIV strain diversity with respect to the vaccine response. We show here that rapid population-level viral adaptation can lead to decreased overall vaccine efficacy and substantially fewer infections averted by vaccination, when comparing scenarios with and without viral evolution (depending on vaccination coverage, vaccine efficacy against the sensitive allele, and the initial resistant allele frequency). Translating this to the epidemic in South Africa, a scenario with 70% vaccination coverage may result in 250,000 new infections within 10 years of vaccine rollout that are due solely to HIV adaptation, all else being equal. These findings suggest that approaches to HIV vaccine development, program implementation, and epidemic modeling may require attention to viral evolutionary responses to vaccination.

evolutionary biology↗

bioRxiv2017

The evolution of queen control over worker reproduction in the social Hymenoptera

A trademark of eusocial insect species is reproductive division of labor, in which workers forego their own reproduction while the queen produces almost all offspring. The presence of the queen is key for maintaining social harmony, but the specific role of the queen in the evolution of eusociality remains unclear. A long-discussed scenario is that a queen either behaviorally or chemically sterilizes her workers. However, the demographic and ecological conditions that enable such manipulation are unknown. Accordingly, we propose a simple model of evolutionary dynamics that is based on haplodiploid genetics. We consider a mutation that acts in a queen, causing her to control the reproductive behavior of her workers. Our mathematical analysis yields precise conditions for the evolutionary emergence and stability of queen-induced worker sterility. These conditions do not depend on the queen's mating frequency. Moreover, we find that queen control is always established if it increases colony reproductive efficiency and can evolve even if it decreases colony efficiency. We further outline the conditions under which queen control is evolutionarily stable against invasion by mutant, reproductive workers.

evolutionary biology↗

bioRxiv2017

Evolutionary dynamics of male reproductive genes in the Drosophila virilis subgroup

Postcopulatory sexual selection (PCSS) is a potent evolutionary force that can drive rapid changes of reproductive genes within species, and thus has the potential to generate reproductive incompatibilities between species. Male seminal fluid proteins (SFPs) are major players in postmating interactions, and likely the main targets of PCSS in males. The virilis subgroup of Drosophila exhibits strong interspecific gametic incompatibilities, and can serve as a model to study the genetic basis of PCSS and gametic isolation. However, reproductive genes in this group have not been characterized. Here we use short-read RNA sequencing of male reproductive organs to examine the evolutionary dynamics of reproductive genes in members of the virilis subgroup: D. americana, D. lummei, D. novamexicana, and D. virilis. For each of the three male reproductive organs (accessory glands, ejaculatory bulb, and testes), we identify genes that show strong expression bias in a given tissue relative to the remaining tissues. We find that the majority of male reproductive transcripts are testes-biased, accounting for ~15% of all annotated genes. Ejaculatory bulb-biased transcripts largely code for lipid metabolic enzymes, and contain orthologs of the D. melanogaster ejaculatory bulb protein, Peb-me, which is involved in mating-plug formation. In addition, we identify 71 candidate SFPs, and show that this set of genes has the highest rate of nonsynonymous codon substitution relative to testes- and ejaculatory bulb-biased genes. Furthermore, these SFPs are underrepresented on the X chromosome and are enriched for proteolytic enzymes, which is consistent with SFPs in other insect species. Surprisingly, we find 35 D. melanogaster SFPs with conserved accessory gland expression in the virilis group, suggesting these genes may have conserved reproductive roles in Drosophila. Finally, we show that several of the SFPs that have the highest rate of nonsynonymous codon substitutions reside on the centromeric half of chromosome 2, which contributes to paternal gametic incompatibility between species. Our results suggest that SFPs are under strong selection in the virilis group, and likely play a major role in PCSS and/or gametic isolation.

evolutionary biology↗

bioRxiv2017

Clay-induced DNA double-strand breaks underlay genetic diversity, antibiotic resistance and molecular basis of asbestosis

Some natural clays and synthetic nanofibres present in the environment have a severe impact on human health. After several decades of research, the molecular mechanism of how asbestos induce cancers is not well understood. Different fibres, including asbestos, can penetrate the membrane and introduce DNA in both, bacterial and eukaryotic cells. Incubating Escherichia coli with sepiolite, a clayey material, and asbestos under friction forces, both fibres cause double-strand breaks in bacteria. Since antibiotics and clays are used together in animal husbandry, the mutagenic effect of these fibres might constitute a pathway to antibiotic resistance due to the friction provided by peristalsis of the gut from farm animals in addition to the previously proposed horizontal gene transfer. Moreover, we raise the possibility that the same mechanism could generate bacteria diversity in natural scenarios with a role in the evolution of species. Finally, we provide a new model on how asbestos may promote mutagenesis and cancer based on the observed mechanical genotoxicity.

evolutionary biology↗

bioRxiv2017

Bacterial tail anchors can target to the mitochondrial outer membrane

During the generation and evolution of the eukaryotic cell, a proteobacterial endosymbiont was refashioned into the mitochondrion, an organelle that appears to have been present in the ancestor of all present-day eukaryotes. Mitochondria harbor proteomes derived from coding information located both inside and outside the organelle, and the rate-limiting step toward the formation of eukaryotic cells may have been development of an import apparatus allowing protein entry to mitochondria. Currently, a widely conserved translocon allows proteins to pass from the cytosol into mitochondria, but how proteins encoded outside of mitochondria were first directed to these organelles at the dawn of eukaryogenesis is not clear. Because several proteins targeted by a carboxyl-terminal tail anchor (TA) appear to have the ability to insert spontaneously into the mitochondrial outer membrane (OM), it is possible that self-inserting, tail-anchored polypeptides obtained from bacteria might have formed the first gate allowing proteins to access mitochondria from the cytosol. Here, we tested whether bacterial TAs are capable of targeting to mitochondria. In a survey of proteins encoded by the proteobacterium Escherichia coli, predicted TA sequences were directed to specific subcellular locations within the yeast Saccharomyces cerevisiae. Importantly, TAs obtained from DUF883 family members ElaB and YqjD were abundantly localized to and inserted at the mitochondrial OM. Our results support the notion that eukaryotic cells are able to utilize membrane-targeting signals present in bacterial proteins obtained by lateral gene transfer, and our findings make plausible a model in which mitochondrial protein translocation was first driven by tail-anchored proteins.

evolutionary biology↗