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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↗

bioRxiv2017

Genome-scale detection of positive selection in 9 primates predicts human-virus evolutionary conflicts

Hotspots of rapid genome evolution hold clues about human adaptation. Here, we present a comparative analysis of nine whole-genome sequenced primates to identify high-confidence targets of positive selection. We find strong statistical evidence for positive selection acting on 331 protein-coding genes (3%), pinpointing 934 adaptively evolving codons (0.014%). Our stringent procedure and quality control of alignments and evolutionary inferences reveal substantial artefacts (20% of initial predictions) that have inflated previous estimates of positive selection, the large majority relating to transcript definitions (61%) or gene models (38%). Our final set of 331 positively selected genes (PSG) are strongly enriched for innate and adaptive immune functions, secreted and cell membrane proteins (e.g. pattern recognition, complement, cytokine pathways, defensins, immune receptors, MHC, Siglecs). We also find evidence for positive selection in reproduction, chromosome segregation and meiosis (e.g. centromere-associated CENPO, CENPT), apolipoproteins, smell/taste receptors, and proteins interacting with mitochondrial-encoded molecules. Focusing on the virus-host interaction, we retrieve most evolutionary conflicts known to influence antiviral activity (e.g. TRIM5, MAVS, SAMHD1, tetherin) and predict 70 novel cases through integration with virus-host interaction data (virus-human PPIs, immune cell expression, infection screens). Protein structure analysis identifies positive selection in the interaction interfaces between viruses and their human cellular receptors (CD4 - HIV; CD46 [MCP] - measles, adenoviruses; CD55 [DAF] - picornaviruses). Finally, the primate PSG consistently show high sequence variation in human exomes, suggesting ongoing evolution. Our curated dataset of positively selected genes and positions, available at http://www.cmbi.umcn.nl/[~]rvdlee/positive_selection/, is a rich source for studying the genetics underlying human (antiviral) phenotypes.

evolutionary biology↗

bioRxiv2017

The Evolution Of Covert Signaling

Human sociality depends upon the benefits of mutual aid and extensive communication. However, diverse norms and preferences complicate mutual aid, and ambiguity in meaning hinders communication. Here we demonstrate that these two problems can work together to enhance cooperation through the strategic use of deliberately ambiguous signals: covert signaling. Covert signaling is the transmission of information that is accurately received by its intended audience but obscured when perceived by others. Such signals may allow coordination and enhanced cooperation while also avoiding the alienation or hostile reactions of individuals with different preferences. Although the empirical literature has identified potential mechanisms of covert signaling, such as encryption in humor, there is to date no formal theory of its dynamics. We introduce a novel mathematical model to assess when a covert signaling strategy will evolve, as well as how receiver attitudes coevolve with covert signals. Covert signaling plausibly serves an important function in facilitating within-group cooperative assortment by allowing individuals to pair up with similar group members when possible and to get along with dissimilar ones when necessary. This mechanism has broad implications for theories of signaling and cooperation, humor, social identity, political psychology, and the evolution of human cultural complexity.

evolutionary biology↗

bioRxiv2017

Meiotic Genes In Colpodean Ciliates Support Secretive Sexuality

Colpodean ciliates potentially pose a problem to macro-organismic theories of evolution: they are putatively asexual and extremely ancient, and yet there is one apparently derived sexual species. If macro-organismic theories of evolution also broadly apply to microbial eukaryotes, though, then most or all of the colpodean ciliates should merely be secretively sexual. Here we show using de novo genome sequencing, that colpodean ciliates have the meiotic genes required for sex and these genes are under functional constraint. Along with these genomic data, we argue that these ciliates are sexual given the cytological observations of both micronuclei and macronuclei within their cells, and the behavioral observations of brief fusions as if the cells were mating. The challenge that colpodean ciliates pose is therefore not to evolutionary theory, but to our ability to induce microbial eukaryotic sex in the laboratory.\n\nContact: dunthorn@rhrk.uni-kl.de

evolutionary biology↗

bioRxiv2017

Disparity, Diversity, And Duplications In The Caryophyllales

O_LIThe role whole genome duplication (WGD) plays in the history of lineages is actively debated. WGDs have been associated with advantages including superior colonization, various adaptations, and increased effective population size. However, the lack of a comprehensive mapping of WGDs within a major plant clade has led to uncertainty regarding the potential association of WGDs and higher diversification rates.\nC_LIO_LIUsing seven chloroplast and nuclear ribosomal genes, we constructed a phylogeny of 5,036 species of Caryophyllales, representing nearly half of the extant species. We phylogenetically mapped putative WGDs as identified from analyses on transcriptomic and genomic data and analyzed these in conjunction with shifts in climatic niche and lineage diversification rate.\nC_LIO_LIThirteen putative WGDs and twenty-seven diversification shifts could be mapped onto the phylogeny. Of these, four WGDs were concurrent with diversification shifts, with other diversification shifts occurring at more recent nodes than WGDs. Five WGDs were associated with shifts to colder climatic niches.\nC_LIO_LIWhile we find that many diversification shifts occur after WGDs it is difficult to consider diversification and duplication to be tightly correlated. Our findings suggest that duplications may often occur along with shifts in either diversification rate, climatic niche, or rate of evolution.\nC_LI

evolutionary biology↗

bioRxiv2017

Experimental Evidence That Thermal Selection Shapes Mitochondrial Genome Evolution

Mitochondria are essential organelles, found within eukaryotic cells, which contain their own DNA. Mitochondrial DNA (mtDNA) has traditionally been used in population genetic and biogeographic studies as a maternally-inherited and evolutionary-neutral genetic marker. However, it is now clear that polymorphisms within the mtDNA sequence are routinely non-neutral, and furthermore several studies have suggested that such mtDNA polymorphisms are also sensitive to thermal selection. These observations led to the formulation of the \"mitochondrial climatic adaptation\" hypothesis, for which all published evidence to date is correlational. Here, we use laboratory-based experimental evolution in the fruit fly, Drosophila melanogaster, to test whether thermal selection can shift population frequencies of two mtDNA haplogroups whose natural frequencies exhibit clinal associations with latitude along the Australian east-coast. We present experimental evidence that the thermal regime in which the laboratory populations were maintained, drove changes in haplogroup frequencies across generations. Our results strengthen the emerging view that intra-specific mtDNA variants are sensitive to selection, and suggest spatial distributions of mtDNA variants in natural populations of metazoans might reflect adaptation to climatic environments rather than within-population coalescence and diffusion of selectively-neutral haplotypes across populations.\n\nImpact SummaryWe applied experimental laboratory evolution to provide the first direct test of the \"mitochondrial climatic hypothesis,\" which predicts that the variation of mitochondrial genomes across natural distributions of metazoans can be shaped by thermal selection. Our design is the first of its kind when it comes to inferring the role of thermal selection in shaping mtDNA frequencies in nature. We harness two naturally occurring mtDNA haplotypes of Drosophila melanogaster that segregate along the east coast of Australia. One of these haplotypes predominates at sub-tropical northern latitudes and the other in the temperate and cooler south of the country. We then compete these haplotypes against each other in replicated experimental fly populations submitted to one of four different thermal regimes, in either the presence or absence of infection by Wolbachia, a coevolved endosymbiont that also exhibits maternal transmission.\n\nWe confirm that when evolving in the laboratory under warmer conditions, a haplotype naturally predominating in subtropical conditions outcompetes a haplotype that predominates at cooler Australian latitudes in the wild. We see this effect on haplotype frequencies in females in populations where latent Wolbachia infections had been purged.\n\nOur results also suggest that sex-specificity of mtDNA effects, and co-occurrence of other maternally-inherited microbiotic entities - of which Wolbachia is just one example - are likely to shape the trajectories of mitochondrial genome evolution in the wild.

evolutionary biology↗

bioRxiv2017

Exon-Based Phylogenomics Strengthens The Phylogeny Of Neotropical Cichlids And Identifies Remaining Conflicting Clades (Cichlomorphae: Cichlidae: Cichlinae)

The phenotypic, geographic, and species diversity of cichlid fishes have made them a group of great interest for studying evolutionary processes. Here we present a targeted-exon next-generation sequencing approach for investigating the evolutionary relationships of cichlid fishes (Cichlidae), with focus on the Neotropical subfamily Cichlinae using a set of 923 primarily single-copy exons designed through mining of the Nile tilapia (Oreochromis niloticus) genome. Sequence capture and assembly were robust, leading to a complete dataset of 415 exons for 139 species (147 terminals) that consisted of 128 Neotropical species, six African taxa, and five Indo-Malagasy cichlids. Gene and species trees were calculated using alternative partitioning schemes and reconstruction methods. In general, all methods yielded similar topologies to previously hypothesized relationships within the Cichlinae and clarified several relationships that were previously poorly supported or in conflict. Additional work will be needed to fully resolve all aspects of Cichlinae phylogeny. Overall, this approach yielded a well-resolved phylogeny of Neotropical cichlids that will be of utility for future assessments of the evolutionary and ecological processes within this diverse group of fishes. Furthermore, the general methodology employed here of exon targeting and capture should be applicable to any group of organisms with the availability of a reference genome.

evolutionary biology↗

bioRxiv2017

Is It Time To Retire Wolbachia Multilocus Sequence Typing (MLST)?

Wolbachia (Alphaproteobacteria, Rickettsiales) is the most common, and arguably one of the most important inherited symbionts. Molecular differentiation of Wolbachia strains is routinely performed with a set of five multilocus sequence typing (MLST) markers. However, since its inception in 2006, the performance of MLST in Wolbachia strain typing has not been assessed objectively. Here, we evaluate the properties of Wolbachia MLST markers and compare it to 252 other single copy loci present in the genome of most Wolbachia strains. Specifically, we investigated how well MLST performs at strain differentiation, at reflecting genetic diversity of strains, and as phylogenetic marker. We find that MLST loci are outperformed by other loci at all tasks they are currently employed for, and thus that they do not reflect the properties of a Wolbachia strain very well. We argue that whole genome typing approaches should be used for Wolbachia typing in the future. Alternatively, if few-loci-approaches are necessary, we provide a characterization of 252 single copy loci for a number a criteria, which may assist in designing specific typing systems or phylogenetic studies.

evolutionary biology↗

bioRxiv2017

Predicting Morphological Disparities In Sea Urchin Skeleton Growth And Form

Sea urchins exhibit among their many species remarkable diversity in skeleton form (e.g., from spheroid to discoid shapes). However, we still do not understand how some related species show distinct morphologies despite inherent similarities at the genetic level. For this, we use theoretical morphology to disentangle the ontogenic processes that play a role in skeletal growth and form. We developed a model that simulates these processes involved and predicted trajectory obtaining 94% and 77% accuracies. We then use the model to understand how morphologies evolved by exploring the individual effects of three structures (ambulacral column, plate number, and polar regions). These structures have changed over evolutionary time and trends indicate they may influence skeleton shape, specifically height-to-diameter ratio, h:d. Our simulations confirm the trend observed but also show how changes in the attributes affect shape; we show that widening the ambulacral column or increasing plate number in columns produces a decrease in h:d (flattening); whereas increasing apical system radius to column length ratio produces an increase in h:d (gloublar shape). Computer simulated h:d matched h:d measured from real specimens. Our findings provide the first explanation of how small changes in these structures can create the diversity in skeletal morphologies.

evolutionary biology↗

bioRxiv2017

Convergent evolution of the army ant syndrome and congruence in big-data phylogenetics

The evolution of the suite of morphological and behavioral adaptations underlying the ecological success of army ants has been the subject of considerable debate. This \"army ant syn-drome\" has been argued to have arisen once or multiple times within the ant subfamily Dorylinae. To address this question I generated data from 2,166 loci and a comprehensive taxon sampling for a phylogenetic investigation. Most analyses show strong support for convergent evolution of the army ant syndrome in the Old and New World but certain relationships are sensitive to analytics. I examine the signal present in this data set and find that conflict is diminished when only loci less likely to violate common phylogenetic model assumptions are considered. I also provide a temporal and spatial context for doryline evolution with timecalibrated, biogeographic, and diversification rate shift analyses. This study underscores the need for cautious analysis of phylogenomic data and calls for more efficient algorithms employing better-fitting models of molecular evolution.\n\nSignificanceRecent interpretation of army ant evolution holds that army ant behavior and morphology originated only once within the subfamily Dorylinae. An inspection of phylogenetic signal in a large new data set shows that support for this hypothesis may be driven by bias present in the data. Convergent evolution of the army ant syndrome is consistently supported when sequences violating assumptions of a commonly used model of sequence evolution are excluded from the analysis. This hypothesis also fits with a simple scenario of doryline biogeography. These results highlight the importance of careful evaluation of signal and conflict within phylogenomic data sets, even when taxon sampling is comprehensive.

evolutionary biology↗

bioRxiv2017

Experimental signal dissection and method sensitivity analyses reaffirm the potential of fossils and morphology in the resolution of seed plant phylogeny

The placement of angiosperms and Gnetales in seed plant phylogeny remains one of the most enigmatic problems in plant evolution, with morphological analyses (which have usually included fossils) and molecular analyses pointing to very distinct topologies. Almost all morphology-based phylogenies group angiosperms with Gnetales and certain extinct seed plant lineages, while most molecular phylogenies link Gnetales with conifers. In this study, we investigate the phylogenetic signal present in published seed plant morphological datasets. We use parsimony, Bayesian inference, and maximum likelihood approaches, combined with a number of experiments with the data, to address the morphological-molecular conflict. First, we ask whether the lack of association of Gnetales with conifers in morphological analyses is due to an absence of signal or to the presence of competing signals, and second, we compare the performance of parsimony and model based approaches with morphological datasets. Our results imply that the grouping of Gnetales and angiosperms is largely the result of long branch attraction, consistent across a range of methodological approaches. Thus, there is a signal for the grouping of Gnetales with conifers in morphological matrices, but it was swamped by convergence between angiosperms and Gnetales, both situated on long branches. However, this effect becomes weaker in more recent analyses, as a result of addition and critical reassessment of characters. Even when a clade including angiosperms and Gnetales is still weakly supported by parsimony, model-based approaches favor a clade of Gnetales and conifers, presumably because they are more resistant to long branch attraction. Inclusion of fossil taxa weakens rather than strengthens support for a relationship of angiosperms and Gnetales. Our analyses finally reconcile morphology with molecules in favoring a relationship of Gnetales to conifers, and show that morphology may therefore be useful in reconstructing other aspects of the phylogenetic history of the seed plants.

evolutionary biology↗

bioRxiv2017

Mitochondrial pseudogenes suggest repeated inter-species hybridization in hominid evolution.

The hypothesis that the evolution of humans involved hybridization between diverged species has been actively debated in recent years. We present novel evidence in support of this hypothesis: the analysis of nuclear pseudogenes of mtDNA (\"NUMTs\"). NUMTs are considered \"mtDNA fossils\", as they preserve sequences of ancient mtDNA and thus carry unique information about ancestral populations. Our comparison of a NUMT sequence shared by humans, chimpanzees, and gorillas with their mtDNAs implies that, around the time of divergence between humans and chimpanzees, our evolutionary history involved the interbreeding of individuals whose mtDNA had diverged as much as ~4.5 Myr prior. This large divergence suggests a distant interspecies hybridization. Additionally, analysis of two other NUMTs suggests that such events occurred repeatedly. Our findings suggest a complex pattern of speciation in primate human ancestors and provide a potential explanation for the mosaic nature of fossil morphology found at the emergence of the hominin lineage.

evolutionary biology↗

bioRxiv2017

Parallel Altitudinal Clines Reveal Adaptive Evolution Of Genome Size In Zea mays

While the vast majority of genome size variation in plants is due to differences in repetitive sequence, we know little about how selection acts on repeat content in natural populations. Here we investigate parallel changes in intraspecific genome size and repeat content of domesticated maize (Zea mays) landraces and their wild relative teosinte across altitudinal gradients in Mesoamerica and South America. We combine genotyping, low coverage whole-genome sequence data, and flow cytometry to test for evidence of selection on genome size and individual repeat abundance. We find that population structure alone cannot explain the observed variation, implying that clinal patterns of genome size are maintained by natural selection. Our modeling additionally provides evidence of selection on individual heterochromatic knob repeats, likely due to their large individual contribution to genome size. To better understand the phenotypes driving selection on genome size, we conducted a growth chamber experiment using a population of highland teosinte exhibiting extensive variation in genome size. We find weak support for a positive correlation between genome size and cell size, but stronger support for a negative correlation between genome size and the rate of cell production. Reanalyzing published data of cell counts in maize shoot apical meristems, we then identify a negative correlation between cell production rate and flowering time. Together, our data suggest a model in which variation in genome size is driven by natural selection on flowering time across altitudinal clines, connecting intraspecific variation in repetitive sequence to important differences in adaptive phenotypes.\n\nAuthor summaryGenome size in plants can vary by orders of magnitude, but this variation has long been considered to be of little to no functional consequence. Studying three independent adaptations to high altitude in Zea mays, we find that genome size experiences parallel pressures from natural selection, causing a linear reduction in genome size with increasing altitude. Though reductions in repetitive content are responsible for the genome size change, we find that only those individual loci contributing most to the variation in genome size are individually targeted by selection. To identify the phenotype influenced by genome size, we study how variation in genome size within a single teosinte population impacts leaf growth and cell division. We find that genome size variation correlates negatively with the rate of cell division, suggesting that individuals with larger genomes require longer to complete a mitotic cycle. Finally, we reanalyze data from maize inbreds to show that faster cell division is correlated with earlier flowering, connecting observed variation in genome size to an important adaptive phenotype.

evolutionary biology↗

bioRxiv2017

Differential Strengths Of Molecular Determinants Guide Environment Specific Mutational Fates

Under the influence of selection pressures imposed by natural environments, organisms maintain competitive fitness through underlying molecular evolution of individual genes across the genome. For molecular evolution, how multiple interdependent molecular constraints play a role in determination of fitness under different environmental conditions is largely unknown. Here, using Deep Mutational Scanning (DMS), we quantitated empirical fitness of [~]2000 single site mutants of Gentamicin-resistant gene (GmR). This enabled a systematic investigation of effects of different physical and chemical environments on the fitness landscape of the gene. Molecular constraints of the fitness landscapes seem to bear differential strengths in an environment dependent manner. Among them, conformity of the identified directionalities of the environmental selection pressures with known effects of the environments on protein folding proves that along with substrate binding, protein stability is the common strong constraint of the fitness landscape. Our study thus provides mechanistic insights into the molecular constraints that allow accessibility of mutational fates in environment dependent manner.\n\nAuthor SummaryEnvironmental conditions play a central role in both organismal adaptations and underlying molecular evolution. Understanding of environmental effects on evolution of genotype is still lacking a depth of mechanistic insights needed to assist much needed ability to forecast mutational fates. Here, we address this issue by culminating high throughput mutational scanning using deep sequencing. This approach allowed comprehensive mechanistic investigation of environmental effects on molecular evolution. We monitored effects of various physical and chemical environments onto single site mutants of model antibiotic resistant gene. Alongside, to get mechanistic understanding, we identified multiple molecular constraints which contribute to various degrees in determining the resulting survivabilities of mutants. Across all tested environments, we find that along with substrate binding, protein stability stands out as the common strong constraints. Remarkable direct dependence of the environmental fitness effects on the type of environmental alteration of protein folding further proves that protein stability is the major constraint of the gene. So, our findings reveal that under the influence of environmental conditions, mutational fates are channeled by various degrees of strengths of underlying molecular constraints.

evolutionary biology↗

bioRxiv2017

Genome Comparisons Indicate Recent Transfer Of wRi-Like Wolbachia Between Sister Species Drosophila suzukii And D. subpulchrella

Wolbachia endosymbionts may be acquired by horizontal transfer, by introgression through hybridization between closely related species, or by cladogenic retention during speciation. All three modes of acquisition have been demonstrated, but their relative frequency is largely unknown. Drosophila suzukii and its sister species D. subpulchrella harbor Wolbachia, denoted wSuz and wSpc, very closely related to wRi, identified in California populations of D. simulans. However, these variants differ in their induced phenotypes: wRi causes significant cytoplasmic incompatibility (CI) in D. simulans, but CI has not been detected in D. suzukii or D. subpulchrella. Our draft genomes of wSuz and wSpc contain full-length copies of 703 of the 734 single-copy genes found in wRi. Over these coding sequences, wSuz and wSpc differ by only 0.004% (i.e., 28 of 704,883 bp); they are sisters relative to wRi, from which each differs by 0.014-0.015%. Using published data from D. melanogaster, Nasonia wasps and Nomada bees to calibrate relative rates of Wolbachia versus host nuclear divergence, we conclude that wSuz and wSpc are too similar - by at least a factor of 100 - to be plausible candidates for cladogenic transmission. These three wRi-like Wolbachia, which differ in CI phenotype in their native hosts, have different numbers of orthologs of genes postulated to contribute to CI; and the CI loci differ at several nucleotides that may account for the CI difference. We discuss the general problem of distinguishing alternative modes of Wolbachia acquisition, focusing on the difficulties posed by limited knowledge of variation in absolute and relative rates of molecular evolution for host nuclear genomes, mitochondria and Wolbachia.

evolutionary biology↗

bioRxiv2017

Duplication And Sub/Neofunctionalization Of malvolio, An Insect Homolog Of Nramp, In The Subsocial Beetle Nicrophorus vespilloides

Gene duplication has long been thought to play a facilitating role in evolution. With growing numbers of sequenced genomes, increasing numbers of duplicate genes are uncovered with unknown functions. Here we examine malvolio, a gene involved in heavy metal transport but that also affects behavior in honey bees and Drosophila. There is only one copy of malvolio in honey bees and Drosophila despite its different roles. A phylogenetic analysis in insects suggests that malvolio has duplicated multiple times in different orders. To test if the two copies might have different functions, we examined expression levels of malvolio in brain, fat bodies, Malpighian tubules, midgut, ovaries, testes and thoracic musculature in the beetle Nicrophorus vespilloides. We found that mvl1 was expressed in all tissues, with highest expression in fat bodies and relatively lower expression in testes, Malpighian tubules, and brain, and ovaries. Expression of mvl2 differed, with significant expression only seen in brain and midgut. Because malvolio has been implicated in behavior, and these beetles have highly developed parenting behavior, we next examined expression during different behavioral states including virgin, mating, preparing resources for offspring, feeding offspring and post care. We found differing expression patterns for the two copies, with mvl1 increasing in expression during resource preparation and feeding offspring, and mvl2 decreasing in these same states. Given these patterns of expression, we suggest that malvolio in N. vespilloides has experienced sub/neofunctionalization following its duplication, and is evolving differing and tissue-specific roles in behavior and physiology.

evolutionary biology↗