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bioRxiv2015

The Genetic Cost of Neanderthal Introgression

Approximately 2-4% of genetic material in human populations outside Africa is derived from Neanderthals who interbred with anatomically modern humans. Recent studies have shown that this Neanderthal DNA is depleted around functional genomic regions; this has been suggested to be a consequence of harmful epistatic interactions between human and Neanderthal alleles. However, using published estimates of Neanderthal inbreeding and the distribution of mutational fitness effects, we infer that Neanderthals had at least 40% lower fitness than humans on average; this increased load predicts the reduction in Neanderthal introgression around genes without the need to invoke epistasis. We also predict a residual Neanderthal mutational load in non-Africans, leading to a fitness reduction of at least 0.5%. This effect of Neanderthal admixture has been left out of previous debate on mutation load differences between Africans and non-Africans. We also show that if many deleterious mutations are recessive, the Neanderthal admixture fraction could increase over time due to the protective effect of Neanderthal haplotypes against deleterious alleles that arose recently in the human population. This might partially explain why so many organisms retain gene flow from other species and appear to derive adaptive benefits from introgression.

Evolutionary Biology↗

bioRxiv2015

Fitness costs of herbicide resistance across natural populations of the common morning glory, Ipomoea purpurea

Although fitness costs associated with plant defensive traits are widely expected, they are not universally detected, calling into question their generality. Here we examine the potential for life history trade-offs associated with herbicide resistance by examining seed germination, root growth, and above-ground growth across 43 naturally occurring populations of Ipomoea purpurea that vary in their resistance to RoundUp(R), the most commonly used herbicide worldwide. We find evidence for life history trade-offs associated with all three traits; highly resistant populations had lower germination rates, shorter roots and smaller above-ground size. A visual exploration of the data indicated that the type of trade-off may differ among populations. Our results demonstrate that costs of adaptation may be present at stages other than simply the production of progeny in this agricultural weed. Additionally, the cumulative effect of costs at multiple life cycle stages can result in severe consequences to fitness when adapting to novel environments.

Evolutionary Biology↗

bioRxiv2015

Adaptation to an invasive host is collapsing a native ecotype

Locally adapted populations are often used as model systems for the early stages of ecological speciation, but most of these young divergent lineages will never become complete species. While the collapse of incipient species is theoretically common, very few examples have been documented in nature. Here I show that soapberry bugs (Jadera haematoloma) have lost adaptations to their native host plant (Cardiospermum corindum) and are regionally specializing on an invasive host plant (Koelreuteria elegans), collapsing a classic and well-documented example of local adaptation. All populations that were adapted to the native host - including those still found on that host today - are now better adapted to the invasive in multiple phenotypes. Weak differentiation remains in two traits, suggesting that homogenization across the region is incomplete. This study highlights the potential for adaptation to invasive species to disrupt native communities by swamping adaptation to native conditions through maladaptive gene flow.

Evolutionary Biology↗

bioRxiv2015

Modularity and Morphometrics: Error Rates in Hypothesis Testing

The study of modularity in morphological systems has increased in the past twenty years, parallel to the popularization of geometric morphometrics, which has led to the emergence of different criteria for detecting modularity on landmark data. However, compared to usual covariance matrix estimators, Procrustes estimators have properties that hinder their use. Here, we compare different representations of form, focusing on detecting modularity patterns defined a priori; we also compare two metrics: one derived from traditional morphometrics (MHI) and another that emerged in the context of landmark data (RV). Using Anthropoid skulls, we compare these metrics over three representations of form: interlandmark distances, Procrustes residuals, and local shape variables. Over Procrustes residuals, both tests fail to detect modularity patterns, while in remaining representations they show the distinction between early and late development in skull ontogeny. To estimate type I and II error rates, we built covariance matrices of known structure; these tests indicate that, considering both effect and sample sizes, tests using MHI are more robust than those using RV. However, both metrics have low power when used on Procrustes residuals. Thus, we conclude that the influence of development and function is poorly represented on Procrustes estimators for covariance matrices.

Evolutionary Biology↗

bioRxiv2015

Strongly asymmetric hybridization barriers shape the origin of a new polyploid species and its hybrid ancestor

O_LIPremise of the study: Hybridization between diploids and tetraploids can lead to new allopolyploid species, often via a triploid intermediate. Viable triploids are often produced asymmetrically, with greater success observed for \"maternal-excess\" crosses where the mother has a higher ploidy than the father. Here we investigate the evolutionary origins of Mimulus peregrinus, an allohexaploid recently derived from the triploid M. x robertsii, to determine whether reproductive asymmetry has shaped the formation of this new species.\nC_LIO_LIMethods: We used reciprocal crosses between the diploid (M. guttatus) and tetraploid (M. luteus) progenitors to determine the viability of triploid M. x robertsii hybrids resulting from paternal-versus maternal-excess crosses. To investigate whether experimental results predict patterns seen in the field, we performed parentage analyses comparing natural populations of M. peregrinus to its diploid, tetraploid, and triploid progenitors. Organellar sequences obtained from pre-existing genomic data, supplemented with additional genotyping was used to establish the maternal ancestry of multiple M. peregrinus and M. x robertsii populations.\nC_LIO_LIKey results: We find strong evidence for asymmetric origins of M. peregrinus, but opposite to the common pattern, with paternal-excess crosses significantly more successful than maternal-excess crosses. These results successfully predicted hybrid formation in nature: 111 of 114 M. x robertsii individuals, and 27 of 27 M. peregrinus, had an M. guttatus maternal haplotype.\nC_LIO_LIConclusion: This study, which includes the first Mimulus chloroplast genome assembly, demonstrates the utility of parentage analysis through genome skimming. We highlight the benefits of complementing genomic analyses with experimental approaches to understand asymmetry in allopolyploid speciation.\nC_LI

Evolutionary Biology↗

bioRxiv2015

Exploring phylogenomic relationships within Myriapoda: should high matrix occupancy be the goal?

Myriapods are one of the dominant terrestrial arthropod groups including the diverse and familiar centipedes and millipedes. Although molecular evidence has shown that Myriapoda is monophyletic, its internal phylogeny remains contentious and understudied, especially when compared to those of Chelicerata and Hexapoda. Until now, efforts have focused on taxon sampling (e.g., by including a handful of genes in many species) or on maximizing matrix occupancy (e.g., by including hundreds or thousands of genes in just a few species), but a phylogeny maximizing sampling at both levels remains elusive. In this study, we analyzed forty Illumina transcriptomes representing three myriapod classes (Diplopoda, Chilopoda and Symphyla); twenty-five transcriptomes were newly sequenced to maximize representation at the ordinal level in Diplopoda and at the family level in Chilopoda. Eight supermatrices were constructed to explore the effect of several potential phylogenetic biases (e.g., rate of evolution, heterotachy) at three levels of mean gene occupancy per taxon (50%, 75% and 90%). Analyses based on maximum likelihood and Bayesian mixture models retrieved monophyly of each myriapod class, and resulted in two alternative phylogenetic positions for Symphyla, as sister group to Diplopoda + Chilopoda, or closer to Diplopoda, the latter hypothesis having been traditionally supported by morphology. Within centipedes, all orders were well supported, but two nodes remained in conflict in the different analyses despite dense taxon sampling at the family level, situating the order Scolopendromorpha as sister group to a morphologically-anomalous grouping of Lithobiomorpha + Geophilomorpha in a subset of analyses. Interestingly, this anomalous result was obtained for all analyses conducted with the most complete matrix (90% of occupancy), being at odds not only with the sparser but more gene-rich supermatrices (75% and 50% supermatrices) or with the matrices optimizing phylogenegic informativeness and the most conserved genes, but also with previous hypotheses based on morphology, development or other molecular data sets. We discuss the implications of these findings in the context of the ever more prevalent quest for completeness in phylogenomic studies. [Chilopoda; Diplopoda; Symphyla: gene tree; species tree; node calibration; missing data.]

Evolutionary Biology↗

bioRxiv2015

On the importance of being structured: instantaneous coalescence rates and a re-evaluation of human evolution

Most species are structured and influenced by processes that either increased or reduced gene flow between populations. However, most population genetic inference methods ignore population structure and reconstruct a history characterized by population size changes under the assumption that species behave as panmictic units. This is potentially problematic since population structure can generate spurious signals of population size change. Moreover, when the model assumed for demographic inference is misspecified, genomic data will likely increase the precision of misleading if not meaningless parameters. In a context of model uncertainty (panmixia versus structure) genomic data may thus not necessarily lead to improved statistical inference.\n\nWe consider two haploid genomes and develop a theory which explains why any demographic model (with or without population size changes) will necessarily be interpreted as a series of changes in population size by inference methods ignoring structure. We introduce a new parameter, the IICR (inverse instantaneous coalescence rate), and show that it is equivalent to a population size only in panmictic models, and mostly misleading for structured models. We argue that this general issue affects all population genetics methods ignoring population structure. We take the PSMC method as an example and show that it infers population size changes that never took place. We apply our approach to human genomic data and find a reduction in gene flow at the start of the Pleistocene, a major increase throughout the Middle-Pleistocene, and an abrupt disconnection preceding the emergence of modern humans.

Evolutionary Biology↗

bioRxiv2015

Homoeologue expression insights into the basis of growth heterosis at the intersection of ploidy and hybridity in Cyprinidae (Carassius auratus red var. × Cyprinus carpio)

Hybridization and polyploidization are considered important driving forces that form new epigenetic regulations. To study the changing patterns of expression accompanying hybridization and polyploidization, we used RNA-seq and qPCR to investigate global expression and homoeologue expression in diploid and allotetraploid hybrids of Carassius auratus red var. ([female]) (R) and Cyprinus carpio ([male]) (C). By comparing the relative expression levels between the hybrids and their parents, we defined the expression level dominance (ELD) and homoeologue expression bias (HEB) in liver tissue. The results showed that polyploidization contributed to the conversion of homoeologue ELD. In addition, hybridization had more effect on the change in HEB than polyploidization, while polyploidization has been considered to have more effect on the change of global gene expression than hybridization. Meanwhile, similar expression patterns were found in growth-related genes. The results suggested that hybridization and polyploidization result in differential degrees of maternal HEB in the three tissues tested. The results of this study will increase our understanding of the underlying regulation mechanism of rapid growth in diploid hybrids and allotetraploids. The differential degrees of global expression and homoeologue expression contribute to growth heterosis in newly formed hybrids and allotetraploids, ensuring the on-going success of allopolyploid speciation.

Evolutionary Biology↗

bioRxiv2015

Collinearity Analysis of Allotetraploid Gossypium Tomentosum and Gossypium Darwinii

G. tomentosum and G. darwinii are wild allotetraploid cotton species, characterized with many excellent traits including finer fiber fineness, drought tolerance, Fusarium wilt and Verticillium wilt resistance. Based on construction of F2 linkage groups of G. hirsutum ?? G. tomentosum and G. hirsutum x G. darwinii, two genetic linkage maps were compared. As a result we found a total of 7 inversion fragments on chr02, chr05, chr08, chr12, chr14, chr16 and chr25, 3 translocation fragments on chr05, chr14 and chr26. Further comparing the inversion and translocation fragments, we noticed four of seven markers orientation of G. tomentosum consistent with G. hirsutum or G. raimondii, one of seven inversion markers orientation of G. darwinii consistent with G. hirsutummeanwhile one of three translocation marker orientation of G. tomentosum consistent with G. raimondii. The result indicatecompare G. darwinii, G. tomentosum has closer genetic relationship to G. hirsutum. This study will play an important role in understanding the genome structure of G. tomentosum and G. darwinii, and open the doors for further in-depth genome research such as fine mapping, tagging genes of interest from wild relatives and evolutionary study.

Evolutionary Biology↗

bioRxiv2015

Surprisingly weak coordination between leaf structure and function among closely-related tomato species

Natural selection may often favor coordination between different traits, or phenotypic integration, in order to most efficiently acquire and deploy scarce resources. As leaves are the primary photosynthetic organ in plants, many have proposed that leaf physiology, biochemistry, and anatomical structure are coordinated along a functional trait spectrum from fast, resource-acquisitive syndromes to slow, resource-conservative syndromes. However, the coordination hypothesis has rarely been tested at a phylogenetic scale most relevant for understanding rapid adaptation in the recent past or predicting evolutionary trajectories in response to climate change. To that end, we used a common garden to examine genetically-based coordination between leaf traits across 19 wild and cultivated tomato taxa. We found surprisingly weak integration between photosynthetic rate, leaf structure, biochemical capacity, and CO2 diffusion, even though all were arrayed in the predicted direction along a fast-slow spectrum. This suggests considerable scope for unique trait combinations to evolve in response to new environments or in crop breeding. In particular, we find that partially independent variation in stomatal and mesophyll conductance may allow a plant to improve water-use efficiency without necessarily sacrificing maximum photosynthetic rates. Our study does not imply that functional trait spectra or tradeoffs are unimportant, but that the many important axes of variation within a taxonomic group may be unique and not generalizable to other taxa.

Evolutionary Biology↗

bioRxiv2015

Environmental unpredictability and inbreeding depression select for mixed dispersal syndromes

Background: Mixed dispersal syndromes have historically been regarded as bet-hedging mechanisms that enhance survival in unpredictable environments, ensuring that some propagules stay in the maternal environment while others can potentially colonize new sites. However, this entails paying the costs of both dispersal and non-dispersal. Propagules that disperse are likely to encounter unfavorable conditions for establishment, while non-dispersing propagules might form populations of close relatives burdened with inbreeding. Here, we investigate the conditions under which mixed dispersal syndromes emerge and are evolutionarily stable, taking into account the risks of both environmental unpredictability and inbreeding.\n\nResults: Using mathematical and computational modeling we show that high dispersal propensity is favored whenever temporal environmental unpredictability is low and inbreeding depression high, whereas mixed dispersal syndromes are adaptive under conditions of high environmental unpredictability, but more particularly if also inbreeding depression is small. Although pure dispersers can be selected for under some circumstances, mixed dispersal provides the optimal strategy under most parameterizations of our models, indicating that this strategy is likely to be favored under a wide variety of conditions. Furthermore, populations exhibiting any single phenotype go inevitably extinct when environmental and genetic costs are high, whilst mixed strategies can maintain viable populations even under such conditions.\n\nConclusions: Our models support the hypothesis that the interplay between inbreeding depression and environmental unpredictability shapes dispersal syndromes, often resulting in mixed strategies. Moreover, mixed dispersal seems to facilitate persistence whenever conditions are critical or nearly critical for survival.

Evolutionary Biology↗

bioRxiv2015

Whole genome sequencing of 56 Mimulus individuals illustrates population structure and local selection

Across western North America, Mimulus guttatus exists as many local populations adapted to site-specific challenges including salt spray, temperature, water availability, and soil chemistry. Gene flow between locally adapted populations will effect genetic diversity in both local demes and across the larger meta-population. A single population of annual M. guttatus from Iron Mountain, Oregon (IM) has been extensively studied and we here building off this research by analyzing whole genome sequences from 34 inbred lines from IM in conjunction with sequences from 22 Mimulus individuals from across the geographic range. Three striking features of these data address hypotheses about migration and selection in a locally adapted population. First, we find very high intra-population polymorphism (synonymous {pi} = 0.033). Variation outside genes may be even higher, but is difficult to estimate because excessive divergence affects read mapping. Second, IM exhibits a significantly positive genome-wide average for Tajimas D. This indicates allele frequencies are typically more intermediate than expected from neutrality, opposite the pattern observed in other species. Third, IM exhibits a distinctive haplotype structure. There is a genome-wide excess of positive associations between minor alleles; consistent with an important effect of gene flow from nearby Mimulus populations. The combination of multiple data types, including a novel, tree-based analytic method and estimates for structural polymorphism (inversions) from previous genetic mapping studies, illustrates how the balance of strong local selection, limited dispersal, and meta-population dynamics manifests across the genome.

Evolutionary Biology↗

bioRxiv2015

MAGELLAN: a tool to explore small fitness landscapes

1In a fitness landscape, fitness values are associated to all genotypes corresponding to several, potentially all, combinations of a set of mutations. In the last decade, many small experimental fitness landscapes have been partially or completely resolved, and more will likely follow. MAGELLAN is a web-based graphical software to explore small fitness/energy landscapes through dynamic visualization and quantitative measures. It can be used to explore input custom landscapes, previously published experimental landscapes or randomly generated model landscapes.

Evolutionary Biology↗

bioRxiv2015

Isolation-by-Drift: Quantifying the Respective Contributions of Genetic Drift and Gene Flow in Shaping Spatial Patterns of Genetic Differentiation

O_LIPairwise measures of neutral genetic differentiation are supposed to contain information about past and on-going dispersal events and are thus often used as dependent variables in correlative analyses to elucidate how neutral genetic variation is affected by landscape connectivity. However, spatial heterogeneity in the intensity of genetic drift, stemming from variations in population sizes, may inflate variance in measures of genetic differentiation and lead to erroneous or incomplete interpretations in terms of connectivity. Here, we tested the efficiency of two distance-based metrics designed to capture the unique influence of spatial heterogeneity in local drift on genetic differentiation. These metrics are easily computed from estimates of effective population sizes or from environmental proxies for local carrying capacities, and allow us to introduce the hypothesis of Spatial-Heterogeneity-in-Effective-Population-Sizes (SHNe). SHNe can be tested in a way similar to isolation-by-distance or isolation-by-resistance within the classical landscape genetics hypothesis-testing framework.\nC_LIO_LIWe used simulations under various models of population structure to investigate the reliability of these metrics to quantify the unique contribution of SHNe in explaining patterns of genetic differentiation. We then applied these metrics to an empirical genetic dataset obtained for a freshwater fish (Gobio occitaniae).\nC_LIO_LISimulations showed that SHNe explained up to 60% of variance in genetic differentiation (measured as Fst) in the absence of gene flow, and up to 20% when migration rates were as high as 0.10. Furthermore, one of the two metrics was particularly robust to uncertainty in the estimation of effective population sizes (or proxies for carrying capacity). In the empirical dataset, the effect of SHNe on spatial patterns of Fst was five times higher than that of isolation-by-distance, uniquely contributing to 41% of variance in pairwise Fst. Taking the influence of SHNe into account also allowed decreasing the signal-to-noise ratio, and improving the upper estimate of effective dispersal distance.\nC_LIO_LIWe conclude that the use of SHNe metrics in landscape genetics will substantially improve the understanding of evolutionary drivers of genetic variation, providing substantial information as to the actual drivers of patterns of genetic differentiation in addition to traditional measures of Euclidean distance or landscape resistance.\nC_LI

Evolutionary Biology↗

bioRxiv2015

Recent demography drives changes in linked selection across the maize genome

Genetic diversity is shaped by the interaction of drift and selection, but the details of this interaction are not well understood. The impact of genetic drift in a population is largely determined by its demographic history, typically summarized by its long-term effective population size (Ne). Rapidly changing population demographics complicate this relationship, however. To better understand how changing demography impacts selection, we used whole-genome sequencing data to investigate patterns of linked selection in domesticated and wild maize (teosinte). We produce the first whole-genome estimate of the demography of maize domestication, showing that maize was reduced to approximately 5% the population size of teosinte before it experienced rapid expansion post-domestication to population sizes much larger than its ancestor. Evaluation of patterns of nucleotide diversity in and near genes shows little evidence of selection on beneficial amino acid substitutions, and that the domestication bottleneck led to a decline in the efficiency of purifying selection in maize. Young alleles, however, show evidence of much stronger purifying selection in maize, reflecting the much larger effective size of present day populations. Our results demonstrate that recent demographic change -- a hallmark of many species including both humans and crops -- can have immediate and wide-ranging impacts on diversity that conflict with would-be expectations based on Ne alone.

Evolutionary Biology↗

bioRxiv2015

Hybrid dysgenesis in Drosophila simulans associated with a rapid global invasion of the P-element

In a classic example of the invasion of a species by a selfish genetic element, the P-element was horizontally transferred from a distantly related species into Drosophila melanogaster. Despite causing hybrid dysgenesis, a syndrome of abnormal phenotypes that include sterility, the P-element spread globally in the course of a few decades in D. melanogaster. Until recently, its sister species, including D. simulans, remained P-element free. Here, we find a hybrid dysgenesis-like phenotype in the offspring of crosses between D. simulans strains collected in different years; a survey of 181 strains shows that around 20% of strains induce hybrid dysgenesis. Using genomic and transcriptomic data, we show that this dysgenesis-inducing phenotype is associated with the invasion of the P-element. To characterize this invasion temporally and geographically, we survey 631 D. simulans strains collected on three continents and over 27 years for the presence of the P-element. We find that the D. simulans P-element invasion occurred rapidly and nearly simultaneously in the regions surveyed, with strains containing P-elements being rare in 2006 and common by 2014. Importantly, as evidenced by their resistance to the hybrid dysgenesis phenotype, strains collected from the latter phase of this invasion have adapted to suppress the worst effects of the P-element.\n\nAuthor SummarySome genes perform necessary organismal functions, others hijack the cellular machinery to replicate themselves, potentially harming the host in the process. These selfish genes can spread through genomes and species; as a result, eukaryotic genomes are typically saddled with large amounts of parasitic DNA. Here, we chronicle the surprisingly rapid global spread of a selfish transposable element through a close relative of the genetic model, Drosophila melanogaster. We see that, as it spreads, the transposable element is associated with damaging effects, including sterility, but that the flies quickly adapt to the negative consequences of the transposable element.

Evolutionary Biology↗

bioRxiv2015

Strong Selection is Necessary for Evolution of Blindness in Cave Dwellers

Blindness has evolved repeatedly in cave-dwelling organisms, and investigating the loss of sight in cave dwellers presents an opportunity to understand the operation of fundamental evolutionary processes, including drift, selection, mutation, and migration. The observation of blind organisms has prompted many hypotheses for their blindness, including both accumulation of neutral, loss-of-function mutations and adaptation to darkness. Here we model the evolution of blindness in caves. This model captures the interaction of three forces: (1) selection favoring alleles causing blindness, (2) immigration of sightedness alleles from a surface population, and (3) loss-of-function mutations creating blindness alleles. We investigated the dynamics of this model and determined selection-strength thresholds that result in blindness evolving in caves despite immigration of sightedness alleles from the surface. Our results indicate that strong selection is required for the evolution of blindness in cave-dwelling organisms, which is consistent with recent work suggesting a high metabolic cost of eye development.

Evolutionary Biology↗

bioRxiv2015

The Genetic Equidistance Phenomenon at the Proteomic Level

The field of molecular evolution started with the alignment of a few protein sequences in the early 1960s. Among the first results found, the genetic equidistance result has turned out to be the most unexpected. It directly inspired the ad hoc universal molecular clock hypothesis that in turn inspired the neutral theory. Unfortunately, however, what is only a maximum distance phenomenon was mistakenly transformed into a mutation rate phenomenon and became known as such. Previous work studied a small set of selected proteins. We have performed proteome wide studies of 7 different sets of proteomes involving a total of 15 species. All 7 sets showed that within each set of 3 species the least complex species is approximately equidistant in average proteome wide identity to the two more complex ones. Thus, the genetic equidis-tance result is a universal phenomenon of maximum distance. There is a reality of constant albeit stepwise or discontinuous increase in complexity during evolution, the rate of which is what the original molecular clock hypothesis is really about. These results provide additional lines of evidence for the recently proposed maximum genetic diversity (MGD) hypothesis.\n\nAvailability and implementationThe source code repository is publicly available at https://github.com/Sephiroth1st/EquidistanceScript\n\nContacthuangshi@sklmg.edu.cn\n\nSupplementary informationSupplementary data are available online.

Evolutionary Biology↗