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bioRxiv2024

Inverted topologies in sequential fitness landscapes enable evolutionary control

Adaptive populations rarely evolve in a static environment. Therefore, understanding and ultimately controlling the evolution of a population requires consideration of fluctuating selective pressures. The fitness landscape metaphor has long been used as a tool for representing the selective pressures a given environment imposes on a population. Much work has already been done to understand the dynamics of evolution on a single fitness landscape. More recently, evolution on fluctuating or sequentially applied landscapes has come to the fore of evolutionary biology. As more empirical landscapes are described, metrics for describing salient features of paired landscapes will have uses for understanding likely evolutionary dynamics. Currently, Pearson correlation coefficient and collateral sensitivity likelihoods are used to quantify topographical relatedness or dissimilarity of a pair of landscapes. Here, we introduce the edge flip fraction, a new metric for comparing landscapes, which quantifies changes in the directionality of evolution between pairs of fitness landscapes. We demonstrate that the edge flip fraction captures topographical differences in landscapes that traditional metrics may overlook which have important consequences for the trajectories of populations evolving on them. By applying this metric to both empirical and synthetic fitness landscapes, we show that it partially predicts the collateral sensitivity likelihoods and can inform the optimality of drug sequences. We show that optimal drug sequences that keep populations within lower fitness regions require shifts in evolutionary directions, which are quantified by the edge flip fraction. Edge flip fraction complements existing measures and may help researchers understand how populations evolve under changing environmental conditions, and could yield clues in the pursuit of evolutionary control.

evolutionary biology↗

bioRxiv2019

Demographic histories and genome-wide patterns of divergence in incipient species of shorebirds

Understanding how incipient species are maintained with gene flow is a fundamental question in evolutionary biology. Whole genome sequencing of multiple individuals holds great potential to illustrate patterns of genomic differentiation as well as the associated evolutionary histories. Kentish (Charadrius alexandrinus) and the white-faced (C. dealbatus) plovers, which differ in their phenotype, ecology and behaviour, are two incipient species and parapatrically distributed in East Asia. Previous studies show evidence of genetic diversification with gene flow between the two plovers. Under this scenario, it is of great importance to explore the patterns of divergence at the genomic level and to determine whether specific regions are involved in reproductive isolation and local adaptation. Here we present the first population genomic analysis of the two incipient species based on the de novo Kentish plover reference genome and resequenced populations. We show that the two plover lineages are distinct in both nuclear and mitochondrial genomes. Using model-based coalescence analysis, we found that population sizes of Kentish plover increased whereas white-faced plovers declined during the Last Glaciation Period. Moreover, the two plovers diverged allopatrically, with gene flow occurring after secondary contact. This has resulted in low levels of genome-wide differentiation, although we found evidence of a few highly differentiated genomic regions in both the autosomes and the Z-chromosome. This study illustrates that incipient shorebird species with gene flow after secondary contact can exhibit discrete divergence at specific genomic regions and provides basis to further exploration on the genetic basis of relevant phenotypic traits.

evolutionary biology↗

bioRxiv2019

ENABLING STABLE COEXISTENCE BY MODIFYING THE ENVIRONMENT

In this work coexistence is studied using a model based on two classical population models: the quasispecies of Eigen [1] and the daisyworld presented by Watson and Lovelock [2]. It is assumed that species are able to modify the environment. We show that this ability enables the coexistence between, at most, two species in equilibrium. Given an initial population, the problem arises as to determine which of the many equilibrium populations, i.e. extinction, only one species or coexistence of two species, will be reached as a function of the species characteristics, specifically their capacity to modify the environment and the optimal growth rate. These results are obtained under general assumptions, which broadens its applicability to other fields as evolutionary biology and social sciences.

evolutionary biology↗

bioRxiv2026

Ancestral secretory programs underlie the evolution of morphological innovations across Spiralia

Understanding how morphological innovation arise from ancestral genetic and cellular systems remains a major challenge in evolutionary biology. Molluscan shells represent one of the most diverse morphological novelties within Spiralia and have been central to the ecological and evolutionary diversification of molluscs. However, the cellular basis of shell formation and the evolutionary origin of shell-forming cell types remain poorly understood. Here, we present a single-cell transcriptomic atlas of the Pacific oyster (Crassostrea gigas) mantle and show that molluscan shell-forming cell types are evolutionarily recent innovations built upon ancestral epithelial secretory systems of spiralians. We identify five spatially segregated shell-forming epithelial cell types, and demonstrate that larval and adult shell-forming cells are developmentally independent and characterized by transcriptomes enriched for evolutionarily young genes. Cross-species cell-type comparisons further reveal that oyster shell-related genes are embedded within conserved epithelial and secretory programs across spiralians. Together, we propose that a substantial genetic foundation for shell formation was already present in the last common ancestor of Spiralia, and that molluscan shell diversity arose through repeated co-option of ancestral genetic programs coupled with novel genes. Our study provides a framework for understanding how ancient cellular architectures can be repeatedly reconfigured to generate morphological novelty during evolution.

evolutionary biology↗

bioRxiv2022

Fold Evolution by Creative Destruction

Mechanisms by which new protein folds emerge and diverge pose central questions in biological sciences. Incremental mutation and step-wise adaptation explain relationships between topologically similar protein folds. However, the universe of folds is diverse and riotous, suggesting roles of more potent and creative forces. Sequence and structure similarity are observed between topologically distinct folds, indicating that proteins with distinct folds may share common ancestry. We found evidence of common ancestry between three distinct {beta}-barrel folds: OB, SH3 and cradle loop barrel (CLB). The data suggest a mechanism of fold evolution that interconverts SH3, OB and CLB. This mechanism, which we call creative destruction, can be generalized to explain other examples of fold evolution including circular permutation. In creative destruction, an open reading frame duplicates or otherwise merges with another to produce a fused polypeptide. A merger forces two ancestral domains into a new sequence and spatial context. The fused polypeptide can explore folding landscapes that are inaccessible to either of the independent ancestral domains. However, the folding landscapes of the fused polypeptide are not fully independent of those of the ancestral domains. Creative destruction is thus partially conservative in that a daughter fold would inherit some motifs from the ancestral folds. After a merger and refolding, adaptive processes such as mutation and loss of extraneous segments optimize the new daughter fold. SignificanceMechanisms of emergence and early diversification of structured proteins present deep and difficult problems in evolutionary biology. Here we excavate the deepest evolutionary history, found within the translation machinery, which is an ancient molecular fossil and the birthplace of all proteins. We demonstrate common origins of some of the simplest, oldest and most common protein folds. Furthermore, the data suggest a mechanism, that we call creative destruction, that explains at molecular level how simple folds spawn more complex folds. In this mechanism, new folds emerge from old folds via gene duplication, expression, exploration of new folding landscapes and adaptation. Creative destruction explains the facile emergence of complex from simple architectures in a funneled exploration.

evolutionary biology↗

bioRxiv2019

Generalists versus specialists in fluctuating environments: a bet-hedging perspective

Bet-hedging evolves in fluctuating environments because long-term genotype success is determined by geometric mean fitness across generations. However, specialist versus generalist strategies are usually considered in terms of arithmetic mean fitness benefits to individuals, as in habitat or foraging preferences. We model how environmental variability affects phenotypic variation within and among individuals to maximize either long-term arithmetic versus geometric mean fitness. For traits with additive fitness effects within lifetimes (e.g. foraging-related traits), genotypes of similar generalists or diversified specialists perform equally well. However, if fitness effects are multiplicative within lifetimes (e.g. sequential survival probabilities), generalist individuals are always favored, since geometric mean fitness favors greater within-individual phenotypic variation than arithmetic mean fitness does. Interestingly, this conservative bet-hedging effect outcompetes diversifying bet-hedging. These results link behavioral and ecological specialization and earlier models of bet-hedging, and thus apply to a range of natural phenomena from habitat choice to host specificity in parasites.\n\nImpact summaryWhich factors determine whether it is better to be a specialist or a generalist? Environmental fluctuations are becoming larger and more unpredictable across the globe as a result of human-induced rapid environmental change. A key challenge of evolutionary biology is therefore to understand how organisms adapt to such variation within and among generations, and currently represents a knowledge gap in evolutionary theory. Here we focus on how traits evolve when the (changing) environment determines the optimal value of a trait, so that the optimal trait value changes unpredictably over time. Our mathematical model investigates how much variation is optimal in a trait. We expect specialists (low within-individual trait variation) to be favored in stable environments, with generalists (high trait variation) favored in more variable environments. We show that the answer depends on whether we look from the point of view of the individual or all individuals of the same genotype. If an individual does well in the short term, but its offspring all experience a different environment and therefore do badly, the genotype as a whole is in trouble, and will not be favored in the long term. One solution to this problem could be to produce offspring with different trait values, to ensure that at least some of the offspring do well no matter the environmental conditions they grow up in. This \"dont put all your eggs in one basket\" diversification strategy is well-known in some organisms, but how helpful is it if there is also some within-individual (i.e. generalist) trait variation? By answering these questions under various environmental scenarios, we link together many different concepts in evolutionary ecology and animal behavior, increasing our understanding about how organisms may cope with the current changes in environmental conditions around the world.

evolutionary biology↗

bioRxiv2020

Modern, archaeological, and paleontological DNA analysis of a human-harvested marine gastropod (Strombus pugilis) from Caribbean Panama

Although protocols exist for the recovery of ancient DNA from land snail and marine bivalve shells, marine conch shells have yet to be studied from a paleogenomic perspective. We first present reference assemblies for both a 623.7 Mbp nuclear genome and a 15.4 kbp mitochondrial genome for Strombus pugilis, the West Indian fighting conch. We next detail a method to extract and sequence DNA from conch shells and apply it to conch from Bocas del Toro, Panama across three time periods: recently-eaten and discarded (n=3), Late Holocene (984-1258 BP) archaeological midden (n=5), and a mid-Holocene (5711-7187 BP) paleontological fossil coral reef (n=5). These results are compared to control DNA extracted from live-caught tissue and fresh shells (n=5). Using high-throughput sequencing, we were able to obtain S. pugilis nuclear sequence reads from shells across all age periods: up to 92.5 thousand filtered reads per sample in live-caught shell material, 4.57 thousand for modern discarded shells, 12.1 thousand reads for archaeological shells, and 114 reads in paleontological shells. We confirmed authenticity of the ancient DNA recovered from the archaeological and paleontological shells based on 5.7x higher average frequency of deamination-driven misincorporations and 15% shorter average read lengths compared to the modern shells. Reads also mapped to the S. pugilis mitochondrial genome for all but the paleontological shells, with consistent ratios of mitochondrial to nuclear mapped reads across sample types. Our methods can be applied to diverse archaeological sites to facilitate reconstructions of the long-term impacts of human behavior on mollusc evolutionary biology.

evolutionary biology↗

bioRxiv2021

Evolutionary tuning of a key helix drove androgen selectivity

The genetic and biophysical mechanisms by which new protein functions evolve are central concerns in evolutionary biology and molecular evolution. Despite much speculation, we know little about how protein function evolves. Here, we use ancestral proteins to trace the evolutionary history of ligand recognition in a sub-class of steroid receptors (SRs), an ancient family of ligand-regulated transcription factors that enable long-range cellular communication central to multicellular life. The most ancestral members of this family display promiscuous ligand binding due to their large ligand binding pockets, while more recently evolved SRs tend to have smaller cavities. Less obvious, however, are the forces driving the selectivity of highly similar ligands. A key example is the divergence between the progesterone and androgen receptors (PR, AR), which display a high degree of sequence similarity and yet display differential ligand preferences. This work uses the ancestral steroid receptor 2 (AncSR2), the common ancestor of all 3-ketosteroids and the ancestral androgen receptor 1 (AncAR1), the seminal androgen receptor, to explore the biophysical mechanisms that drove the evolution of androgen specificity. We determine that ligand specificity in androgen receptors is driven by changes in the conformational dynamics of the receptor as well as altered binding pocket interactions, with helix 10 (H10) playing a critical role in tuning ligand specificity.

evolutionary biology↗

bioRxiv2022

Differentiation of thermal reaction norms between marginal and core populations of a northward expanding parasitoid

Understanding the speed of and the type of mechanisms that species use to adapt to rapid change is a central question in evolutionary biology. Classically, the two mechanisms denoted in the literature that allow individuals to address these environmental changes are either phenotypic plasticity or rapid evolutionary changes. However, phenotypic plasticity itself can evolve rapidly. In this study, we investigated the genetic differentiation between marginal and core populations of a high-trophic level insect, Leptopilina boulardi, a Drosophila parasitoid, which has exhibited a very rapid progression northward of its geographical range. Several life history traits have been investigated in different populations according to four fluctuating thermal regimes that mimic the thermal conditions in the field. We found that at low developmental temperature, the two northern marginal populations that have to face a colder winter, survive longer than the two core populations. In addition, the northernmost populations exhibit a higher potential fecundity, a higher starvation resistance and a larger amount of energy at low temperatures. These significant genetic differentiations with genotype-by-environment interactions show that a rapid genetic differentiation of the shape of thermal reaction norms is possible when populations have to cope with new environments.

evolutionary biology↗

bioRxiv2023

Relative energetic economy of cleistogamous selfing in three populations of the perennial Ruellia humilis

Premise of researchWhat maintains mixed selfing and outcrossing is an enduring mystery in evolutionary biology. Cleistogamy, where individuals produce both potentially outcrossing chasmogamous and obligately selfing cleistogamous flowers, provides an ideal framework in which to study the evolutionary forces maintaining mixed-mating. Despite their promise for providing insight into mating system evolution, few studies of cleistogamous species have comprehensively investigated the relative costs and benefits of cleistogamous selfing. MethodologyWe quantified the necessary components to calculate the relative energetic cost of reproduction of the different flower types in three natural populations of the perennial Ruellia humilis Nutt (Acanthaceae). These components include flower dry mass, fertility (fruit set), and seed mass and number per fruit. We also measured pollen-ovule ratios for both flower types as another measure of relative energetic investment. We additionally tracked phenology of the two flower types and used the proportion of chasmogamous flowers to estimate maximum potential outcrossing rates. Pivotal ResultsWe found that the energetic cost of reproduction via cleistogamous flowers was about 4-10 times less than that of reproduction via chasmogamous flowers, and this energetic economy was from both reduced mass and increased fertility of cleistogamous flowers. Pollen ovule ratios in cleistogamous flowers were one third to one half those of chasmogamous flowers, providing additional support for their energetic economy. Maximum potential outcrossing rates in these populations based on chasmogamous flower production were between 43-61%, but chasmogamous flowers can autogamously self at rates of 33-75%. ConclusionsThe relative energetic economy of cleistogamous flowers suggest that progeny from chasmogamous flowers would have to have 4-10 times greater relative fitness to explain their evolutionary maintenance. These values are likely even greater considering the reduced investment in pollen production in cleistogamous flowers. Ongoing work will quantify potential advantages of chasmogamous flowers due to inbreeding depression and heterosis.

evolutionary biology↗

bioRxiv2014

Restriction and recruitment - gene duplication and the origin and evolution of snake venom toxins

Snake venom has been hypothesised to have originated and diversified via a process that involves duplication of genes encoding body proteins with subsequent recruitment of the copy to the venom gland, where natural selection acts to develop or increase toxicity. However, gene duplication is known to be a rare event in vertebrate genomes and the recruitment of duplicated genes to a novel expression domain (neofunctionalisation) is an even rarer process that requires the evolution of novel combinations of transcription factor binding sites in upstream regulatory regions. Therefore, whilst this hypothesis concerning the evolution of snake venom is therefore very unlikely and should be regarded with caution, it is nonetheless often assumed to be established fact, hindering research into the true origins of snake venom toxins. To critically evaluate this hypothesis we have generated transcriptomic data for body tissues and salivary and venom glands from five species of venomous and non-venomous reptiles. Our comparative transcriptomic analysis of these data reveals that snake venom does not evolve via the hypothesised process of duplication and recruitment of genes encoding body proteins. Indeed, our results show that many proposed venom toxins are in fact expressed in a wide variety of body tissues, including the salivary gland of non-venomous reptiles and that these genes have therefore been restricted to the venom gland following duplication, not recruited. Thus snake venom evolves via the duplication and subfunctionalisation of genes encoding existing salivary proteins. These results highlight the danger of the elegant and intuitive ?just-so story? in evolutionary biology.

Evolutionary Biology↗

bioRxiv2026

Rapid speciation in Harlequin Toads (Anura: Bufonidae) endemic to the Sierra Nevada de Santa Marta

The Neotropical genus Atelopus has experienced a drastic population decline in recent decades. Despite this, a knowledge gap remains regarding the conservation genetic status, phylogeography, and demographic history of most of its species, especially those endemic to areas with limited access like the Sierra Nevada de Santa Marta in Colombia. In this genomic study, we inferred phylogenetic relationships, demographic history, and gene flow among four endemic Atelopus morphospecies in the Sierra Nevada de Santa Marta-SNSM. Additionally, we compared the effective population size (Ne) estimates with the available population census data. NextRAD was used to obtain genomic data from 95 individuals collected at five sites in the SNSM and two in the Colombian Pacific (outgroup). The morphospecies recently diverged in a scenario without gene flow and were recovered as monophyletic. Their phylogenetic relationships were discordant, which is attributed to the presence of incomplete lineage sorting-ILS, which would also explain their shared ancestry among them. The lack of gene flow as well as the recent divergence times given by demography suggests a recent and rapid speciation. However, the reproductive isolation mechanisms that promote or maintain the species boundaries in this group remain unknown and require further investigation. We suggest that this process may have been influenced by the complex topography of the SNSM, traits such as high philopatry, low dispersal ability, and behavioral factors such as habitat preference or to factors related to genetic architecture that influenced the rapid formation of reproductive barriers among populations. Additionally, a pattern of population decline was observed around 200.000 years ago, with recent increases in three morphospecies. Despite the reduction in effective population size, no signs of inbreeding were detected. However, for A. laetissimus, the only species surveyed, the estimated value of Ne and its implications should be interpreted with caution. Ultimately, our findings reveal an evolutionary history shaped by a burst of diversification and abrupt reproductive isolation, highlighting how the resulting endemism and restricted genetic connectivity shape the unique evolutionary trajectory and vulnerability of this threatened montane species. Significance StatementThe mechanisms driving rapid speciation in montane ecosystems remain a central question in evolutionary biology. This study provides crucial genomic insights into the diversification of four endemic Atelopus species in an isolated Neotropical massif. We reveal a compelling evolutionary scenario where species diverge rapidly in absence of gene flow. This rapid speciation was likely facilitated by complex topography, environmental heterogeneity, and ecological and behavioral differences among species. Nevertheless, the evolutionary processes that limited gene flow among SNSM species have not yet been identified.

evolutionary biology↗

bioRxiv2022

Coevolution of reproducers and replicators at the origin of life and the conditions for the origin of genomes

There are two fundamentally distinct but inextricably linked types of biological evolutionary units, reproducers and replicators. Reproducers are cells and organelles that reproduce via various forms of division and maintain the physical continuity of compartments and their content. Replicators are genetic elements (GE), including genomes of cellular organisms and various autonomous elements, that both cooperate with reproducers and rely on the latter for replication. All known cells and organisms comprise a union between replicators and reproducers. We explore a model in which cells emerged via symbiosis between primordial metabolic reproducers (protocells) which evolved, on short time scales, via a primitive form of selection and random drift, and mutualist replicators. Mathematical modeling identifies the conditions, under which GE-carrying protocells can outcompete GE-less ones, taking into account that, from the earliest stages of evolution, replicators split into mutualists and parasites. Analysis of the model shows that, for the GE-containing protocells to win the competition and to be fixed in evolution, it is essential that the birth-death process of the GE is coordinated with the rate of protocell division. At the early stages of evolution, random, high-variance cell division is advantageous compared to symmetrical division because the former provides for the emergence of protocells containing only mutualists, preventing takeover by parasites. These findings illuminate the likely order of key events on the evolutionary route from protocells to cells that involved the origin of genomes, symmetrical cell division and anti-parasite defense systems. SignificanceThe origin of life, which is equivalent to the origin of cells, is arguably the greatest enigma in biology. The remarkable complexity characteristic of even the simplest extant cells could only evolve from simpler, pre-biological entities. Reconstructing that pre-cellular stage of evolution is a hard challenge. We present an evolutionary scenario in which cells evolved via symbiosis between protocells that harbored protometabolic reaction networks, could divide and were subject to selection, but lacked genomes, and primordial genetic elements. Mathematical modeling reveals conditions for the survival of such symbionts and the origin of modern-type genomes, in particular, coordination of the rates of protocell division and replication of genetic elements as well as random division of protocells.

evolutionary biology↗

bioRxiv2014

SpeciesGeoCoder: Fast categorisation of species occurrences for analyses of biodiversity, biogeography, ecology and evolution

Understanding the patterns and processes underlying the uneven distribution of biodiversity across space and time constitutes a major scientific challenge in evolutionary biology. With rapidly accumulating species occurrence data, there is an increasing need for making the process of coding species into operational units for biogeographic and evolutionary analyses faster, automated, transparent and reproducible. Here we present SpeciesGeoCoder, a free software package written in Python and R, that allows for easy coding of species into user-defined areas. These areas may be of any size and be purely geographical (i.e., polygons) such as political units, conservation areas, biomes, islands, biodiversity hotspots, and areas of endemism, but may also include altitudinal ranges. This flexibility allows scoring species into complex categories, such as those encountered in topographically and ecologically heterogeneous landscapes. In addition, SpeciesGeoCoder can be used to facilitate sorting and cleaning of occurrence data. The various outputs of SpeciesGeoCoder include quantitative biodiversity statistics, global and local distribution maps, and NEXUS files that can be directly used in many phylogeny-based applications for ancestral state reconstruction, investigations on biome evolution, and diversification rate analyses. Our simulations indicate that even datasets containing hundreds of millions of records can be analysed in relatively short time using a regular desktop computer. We exemplify the use of our program through two contrasting examples: i) inferring historical dispersal of birds across the Isthmus of Panama, separating lowland vs. montane species and optimising the results onto a species-level, dated phylogeny; and ii) exploring seasonal variations in the occurrence of 10 GPS-tracked individuals of moose (Alces alces) over one year in northern Sweden. These analyses show that SpeciesGeoCoder allows an easy, flexible and fast categorisation of species distribution data for various analyses in ecology and evolution, with potential use at different spatial, taxonomic and temporal scales.

Evolutionary Biology↗

bioRxiv2020

Behavioral and genomic sensory adaptations underlying the pest activity of Drosophila suzukii

Studying how novel phenotypes originate and evolve is fundamental to the field of evolutionary biology as it allows us to understand how organismal diversity is generated and maintained. However, determining the basis of novel phenotypes is challenging as it involves orchestrated changes at multiple biological levels. Here, we aim to overcome this challenge by using a comparative species framework combining behavioral, gene expression, and genomic analyses to understand the evolutionary novel egg-laying substrate-choice behavior of the invasive pest species Drosophila suzukii. First, we used egg-laying behavioral assays to understand the evolution of ripe fruit oviposition preference in D. suzukii as compared to closely related species D. subpulchrella and D. biarmipes, as well as D. melanogaster. We show that D. subpulchrella and D. biarmipes lay eggs on both ripe and rotten fruits, suggesting that the transition to ripe fruit preference was gradual. Secondly, using two-choice oviposition assays, we studied how D. suzukii, D. subpulchrella, D. biarmipes and D. melanogaster differentially process key sensory cues distinguishing ripe from rotten fruit during egg-laying. We found that D. suzukiis preference for ripe fruit is in part mediated through a species-specific preference for stiff substrates. Lastly, we sequenced and annotated a high-quality genome for D. subpulchrella. Using comparative genomic approaches, we identified candidate genes involved in D. suzukiis ability to seek out and target ripe fruits. Our results provide detail to the stepwise evolution of pest activity in D. suzukii, indicating important cues used by this species when finding a host, and the molecular mechanisms potentially underlying their adaptation to a new ecological niche.

evolutionary biology↗

bioRxiv2019

Evolution of barrier loci at an intermediate stage of speciation with gene flow

Understanding the origin of new species is a central goal in evolutionary biology. Diverging lineages often evolve highly heterogeneous patterns of differentiation; however, the underlying mechanisms are not well understood. We used an integrated approach to investigate evolutionary processes governing genetic differentiation between the hybridizing campions (Silene dioica (L.) Clairv. and S. latifolia Poiret). Demographic modeling indicated that the two species diverged with continuous gene flow. The best-supported scenario with heterogeneity in both migration rate and effective population size suggested that 5% of the loci evolved without gene flow. Differentiation (FST) and sequence divergence (dXY) were correlated and both tended to peak in the middle of most linkage groups, consistent with reduced gene flow at highly differentiated loci. Highly differentiated loci further exhibited signatures of selection and differentiation was significantly elevated around previously identified QTLs associated with assortative mating. In between-species population pairs, isolation by distance was stronger for genomic regions with low between-species differentiation than for highly differentiated regions that may contain barrier loci. Moreover, differentiation landscapes within and between species were only weakly correlated suggesting that the interplay of background selection and conserved genomic features is not the dominant determinant of genetic differentiation in these lineages. Instead, our results suggest that divergent selection drove the evolution of barrier loci played and the genomic landscape of differentiation between the two species, consistent with predictions for speciation in the face of gene flow.

evolutionary biology↗

bioRxiv2019

Genetic and genomic analyses reveal boundaries between species closely related to Cryptococcus pathogens

Speciation is a central mechanism of biological diversification. While speciation is well studied in plants and animals, in comparison, relatively little is known about speciation in fungi. One fungal model is the Cryptococcus genus, which is best known for the pathogenic Cryptococcus neoformans/Cryptococcus gattii species complex that causes over 200,000 new infections in humans annually. The closest non-human pathogenic relatives are the sibling species, Cryptococcus amylolentus and Tsuchiyaea wingfieldii. However, because relatively few isolates of each species are available, it is unclear whether they represent divergent lineages of the same species or different biological species. The recent isolation of an additional strain, preliminarily identified as T. wingfieldii, prompted us to reexamine this group as it may inform about the evolutionary processes underlying the diversification of both non-pathogenic and pathogenic Cryptococcus lineages. Using genomic data, we reappraised the phylogenetic relationship of the four available strains and confirmed the genetic separation of C. amylolentus and T. wingfieldii (now Cryptococcus wingfieldii), and revealed an additional cryptic species, for which the name Cryptococcus floricola is proposed. Comparison of full-length chromosome assemblies revealed approximately 6% pairwise sequence divergence between the three species, and identified significant genomic changes, including inversions as well as a reciprocal translocation that involved inter-centromeric ectopic recombination, which together likely impose significant barriers to genetic exchange. Using genetic crosses, we show that while C. wingfieldii cannot interbreed with any of the other strains, C. floricola can undergo sexual reproduction with C. amylolentus. However, most of the spores resulting from this cross were inviable, and many were sterile, indicating that the two species are genetically isolated through intrinsic post-zygotic barriers and possibly due to niche differentiation. Genome sequencing and analysis of the progeny demonstrated decreased recombination frequency during meiosis in heterospecific crosses compared to C. amylolentus conspecific crosses. This study advances our understanding of speciation in fungi and highlights the power of genomics in assisting our ability to correctly identify and discriminate fungal species. Author SummaryThe idea of species as discrete natural units seems rather intuitive for most people, just as cells are the basic units of life. However, when observing variation across a species range, boundaries can become blurred making it less than obvious when different populations evolve into separate species. Additionally, separate species can still interbreed, such as lions breeding with tigers to produce a liger or a tigon (depending on the paternal and maternal species of origin), but the resulting offspring is usually inviable or sterile, which in turn is evidence that the parents involved are distinct species. Therefore, what species are and how they originate is still an open question in evolutionary biology. While recent advances have been made in the fields of animal and plant speciation, many other important components of biological diversity, such as fungi, are still understudied. Genome sequencing is now providing new tools to address the genetic mechanisms that drive divergence and reproductive isolation between populations, including genetic incompatibilities, sequence divergence, and chromosomal rearrangements. Here we focus on the Cryptococcus amylolentus species complex, a non-pathogenic fungal lineage closely related to the human pathogenic Cryptococcus neoformans/Cryptococcus gattii complex. Using genetic and genomic analysis we reexamined the species boundaries of four available isolates within the C. amylolentus complex and revealed three genetically isolated species. The genomes of these species are ~6% divergent and exhibit chromosome rearrangements, including translocations and small-scale inversions. Although two of the species (C. amylolentus and newly described C. floricola) are still able to interbreed, the resulting hybrid progeny were mostly inviable, and many were sterile, indicating that barriers to reproduction have already been established. Our results will foster additional studies addressing the transitions between non-pathogenic and pathogenic Cryptococcus lineages.

evolutionary biology↗

bioRxiv2018

Genome-wide scans of selection highlight the impact of biotic and abiotic constraints in natural populations of the model grass Brachypodium distachyon.

Grasses are essential plants for ecosystem functioning. Quantifying the selective pressures that act on natural variation in grass species is therefore essential regarding biodiversity maintenance. In this study, we investigate the selection pressures that act on two distinct populations of the grass model Brachypodium distachyon without prior knowledge about the traits under selection. We took advantage of whole-genome sequencing data produced for 44 natural accessions of B. distachyon and used complementary genome-wide scans of selection (GWSS) methods to detect genomic regions under balancing and positive selection. We show that selection is shaping genetic diversity at multiple temporal and spatial scales in this species and affects different genomic regions across the two populations. Gene Ontology annotation of candidate genes reveals that pathogens may constitute important factors of positive and balancing selection in Brachypodium distachyon. We eventually cross-validated our results with QTL data available for leaf-rust resistance in this species and demonstrate that, when paired with classical trait mapping, GWSS can help pinpointing candidate genes for further molecular validation. Thanks to a near-base perfect reference genome and the large collection of freely available natural accessions collected across its natural range, B. distachyon appears as a prime system for studies in ecology, population genomics and evolutionary biology.

evolutionary biology↗