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Apoptosis in snowflake yeast: novel trait, or side effect of toxic waste?

Recent experiments evolving de novo multicellularity in yeast have found that large-cluster forming genotypes also exhibit higher rates of programmed cell death (apoptosis). This was previously interpreted as the evolution of a simple form of cellular division of labor: apoptosis results in the scission of cell-cell connections, allowing snowflake yeast to produce proportionally smaller, faster-growing propagules. Through spatial simulations, Duran-Nebreda and Sole (2015) develop the novel null hypothesis that apoptosis is not an adaptation, per se, but is instead caused by the accumulation of toxic metabolites in large clusters. Here we test this hypothesis by synthetically creating unicellular derivatives of snowflake yeast through functional complementation with the ancestral ACE2 allele. We find that multicellular snowflake yeast with elevated apoptosis exhibit a similar rate of apoptosis when cultured as single cells. We also show that larger snowflake yeast clusters tend to contain a greater fraction of older, senescent cells, which may explain why larger clusters of a given genotype are more apoptotic. Our results show that apoptosis is not caused by side effects of spatial structure, such as starvation or waste product accumulation, and are consistent with the hypothesis that elevated apoptosis is a trait which co-evolves with large cluster size.

Evolutionary Biology

Elevation of linkage disequilibrium above neutral expectations in ancestral and derived populations of Drosophila melanogaster

The extent to which selection and demography impact patterns of genetic diversity in natural populations of Drosophila melanogaster is yet to be fully understood. We previously observed that the pattern of LD at scales of ~10 kb in the Drosophila Genetic Reference Panel (DGRP), consisting of 145 inbred strains from Raleigh, North Carolina, measured both between pairs of sites and as haplotype homozygosity, is elevated above neutral demographic expectations. Further, we demonstrated that signatures of strong and recent soft sweeps are abundant. However, the extent to which this pattern is specific to this derived and admixed population is unknown. Neither is it clear whether such a pattern may have arisen as a consequence of the extensive inbreeding performed to generate the DGRP data. Here we analyze > 100 fully sequenced strains from Zambia, an ancestral population to the Raleigh population, that has experienced little to no admixture and was generated by sequencing haploid embryos rather than inbred strains. This data set allows us to determine whether patterns of elevated LD and signatures of abundant soft sweeps are generic to multiple populations of D. melanogaster or whether they are generated either by inbreeding, bottlenecks or admixture in the DGRP dataset. We find an elevation in long-range LD and haplotype homozygosity in the Zambian dataset, confirming the result from the DGRP data set. This elevation in LD and haplotype structure remains even after controlling for many sources of LD in the data including genomic inversions, admixture, population substructure, close relatedness of individual strains, and recombination rate variation. Furthermore, signatures of partial soft sweeps similar to those found in the DGRP are common in Zambia. These results suggest that while the selective forces and sources of adaptive mutations may differ in Zambia and Raleigh, elevated long-range LD and signatures of soft sweeps are generic in D. melanogaster.

Evolutionary Biology

Para-allopatry in hybridizing fire-bellied toads (Bombina bombina and B. variegata): inference from transcriptome-wide coalescence analyses

Ancient origins, profound ecological divergence and extensive hybridization make the fire-bellied toads Bombina bombina and B. variegata (Anura: Bombinatoridae) an intriguing test case of ecological speciation. Narrow Bombina hybrid zones erect barriers to neutral introgression whose strength has been estimated previously. We test this prediction by inferring the rate of gene exchange between pure populations on either side of the intensively studied Krakow transect. We developed a software pipeline to extract high confidence sets of orthologous genes from de novo transcriptome assemblies, fitted a range of divergence models to these data and assessed their relative support with analytic likelihoods calculations. There was clear evidence for post-divergence gene flow, but, as expected, no perceptible signal of recent introgression via the nearby hybrid zone. The analysis of two additional Bombina taxa (B. v. scabra and B. orientalis) validated our parameter estimates against a larger set of prior expectations. Despite substantial cumulative introgression over millions of years, adaptive divergence of the hybridizing taxa is essentially unaffected by their lack of reproductive isolation. Extended distribution ranges also buffer them against small-scale environmental perturbations that have been shown to reverse the speciation process in other, more recent ecotypes.

Evolutionary Biology

The Strength of Selection Against Neanderthal Introgression

Hybridization between humans and Neanderthals has resulted in a low level of Neanderthal ancestry scattered across the genomes of many modern-day humans. After hybridization, on average, selection appears to have removed Neanderthal alleles from the human population. Quantifying the strength and causes of this selection against Neanderthal ancestry is key to understanding our relationship to Neanderthals and, more broadly, how populations remain distinct after secondary contact. Here, we develop a novel method for estimating the genome-wide average strength of selection and the density of selected sites using estimates of Neanderthal allele frequency along the genomes of modern-day humans. We confirm that East Asians had somewhat higher initial levels of Neanderthal ancestry than Europeans even after accounting for selection. We find that the bulk of purifying selection against Neanderthal ancestry is best understood as acting on many weakly deleterious alleles. We propose that the majority of these alleles were effectively neutral--and segregating at high frequency--in Neanderthals, but became selected against after entering human populations of much larger effective size. While individually of small effect, these alleles potentially imposed a heavy genetic load on the early-generation human-Neanderthal hybrids. This work suggests that differences in effective population size may play a far more important role in shaping levels of introgression than previously thought.\n\nAuthor SummaryA small percentage of Neanderthal DNA is present in the genomes of many contemporary human populations due to hybridization tens of thousands of years ago. Much of this Neanderthal DNA appears to be deleterious in humans, and natural selection is acting to remove it. One hypothesis is that the underlying alleles were not deleterious in Neanderthals, but rather represent genetic incompatibilities that became deleterious only once they were introduced to the human population. If so, reproductive barriers must have evolved rapidly between Neanderthals and humans after their split. Here, we show that oberved patterns of Neanderthal ancestry in modern humans can be explained simply as a consequence of the difference in effective population size between Neanderthals and humans. Specifically, we find that on average, selection against individual Neanderthal alleles is very weak. This is consistent with the idea that Neanderthals over time accumulated many weakly deleterious alleles that in their small population were effectively neutral. However, after introgressing into larger human populations, those alleles became exposed to purifying selection. Thus, rather than being the result of hybrid incompatibilities, differences between human and Neanderthal effective population sizes appear to have played a key role in shaping our present-day shared ancestry.

Evolutionary Biology

Age-related and heteroplasmy-related variation in human mtDNA copy number

The mitochondrial (mt) genome is present in many copies in human cells, and intra-individual variation in mtDNA sequences is known as heteroplasmy. Recent studies found that heteroplasmies are highly tissue-specific, site-specific, and allele-specific, however the functional implications have not been explored. This study investigates variation in mtDNA copy numbers (mtCN) in 12 different tissues obtained at autopsy from 152 individuals (ranging in age from 3 days to 96 years). Three different methods to estimate mtCN were compared: shotgun sequencing (in 4 tissues), capture-enriched sequencing (in 12 tissues) and droplet digital PCR (ddPCR, in 2 tissues). The highest precision in mtCN estimation was achieved using shotgun sequencing data. However, capture-enrichment data provide reliable estimates of relative (albeit not absolute) mtCNs. Comparisons of mtCN from different tissues of the same individual revealed that mtCNs in different tissues are, with few exceptions, uncorrelated. Hence, each tissue of an individual seems to regulate mtCN in a tissue-related rather than an individual-dependent manner. Skeletal muscle (SM) samples showed an age-related decrease in mtCN that was especially pronounced in males, while there was an age-related increase in mtCN for liver (LIV) samples. MtCN in SM samples was significantly negatively correlated with both the total number of heteroplasmic sites and with minor allele frequency (MAF) at two heteroplasmic sites, 408 and 16327. Heteroplasmies at both sites are highly specific for SM, accumulate with aging and are part of functional elements that regulate mtDNA replication. These data support the hypothesis that selection acting on these heteroplasmic sites is reducing mtCN in SM of older individuals.\n\nAuthor SummaryThe total number of mitochondrial genomes in a human cell differs between individuals and between the tissues of a single individual; however the factors that influence this variation remain unknown. We estimated mtDNA copy number (mtCN) in 12 different tissues of 152 individuals applying three different methods, and found age-related variation for two tissues: mtCN in skeletal muscle is negatively correlated with age (especially in males) while mtCN in liver is positively correlated with age. Overall, mtCNs of different tissues within an individual are mainly independent of each other, indicating that tissue-specific rather than individual-specific processes largely influence mtCN.\n\nHeteroplasmy refers to intra-individual differences in the sequence of the mtDNA genome and heteroplasmic mutations accumulate during aging. Linear and partial regression analyses of mtCN with heteroplasmy (determined in a previous study of these same samples) revealed that the decrease of mtCN in skeletal muscle is mainly correlated with an increasing total number of heteroplasmic sites, and with increasing minor allele frequency at two sites (408 and 16327), that are heteroplasmic almost exclusively in skeletal muscle. As both sites are part of functional elements required for regulation of mtDNA replication, we suggest that selection may be acting via increasing heteroplasmy to reduce mtCN during aging.

Evolutionary Biology

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

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

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

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

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

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

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

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

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

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

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

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

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