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bioRxiv2016

Differential paralog divergence modulates evolutionary outcomes in yeast

Evolutionary outcomes depend not only on the selective forces acting upon a species, but also on the genetic background. However, large timescales and uncertain historical selection pressures can make it difficult to discern such important background differences between species. Experimental evolution is one tool to compare evolutionary potential of known genotypes in a controlled environment. Here we utilized a highly reproducible evolutionary adaptation in Saccharomyces cerevisiae to investigate whether other yeast species would adopt similar evolutionary trajectories. We evolved populations of S. cerevisiae, S. paradoxus, S. mikatae, S. uvarum, and interspecific hybrids between S. uvarum and S. cerevisiae for ~200-500 generations in sulfate-limited continuous culture. Wild-type S. cerevisiae cultures invariably amplify the high affinity sulfate transporter gene, SUL1. However, while amplification of the SUL1 locus was detected in S. paradoxus and S. mikatae populations, S. uvarum cultures instead selected for amplification of the paralog, SUL2. We measured the relative fitness of strains bearing deletions and amplifications of both SUL genes from different species, confirming that, converse to S. cerevisiae, S. uvarum SUL2 contributes more to fitness in sulfate limitation than S. uvarum SUL1. By measuring the fitness and gene expression of chimeric promoter-ORF constructs, we were able to delineate the cause of this differential fitness effect primarily to the promoter of S. uvarum SUL1. Our data show evidence of differential sub-functionalization among the sulfur transporters across Saccharomyces species through recent changes in noncoding sequence. Furthermore, these results show a clear example of how such background differences due to paralog divergence can drive significant changes in evolutionary trajectories of eukaryotes.

Evolutionary Biology↗

bioRxiv2016

The combinatorics of discrete time-trees: theory and open problems

A time-tree is a rooted phylogenetic tree such that all internal nodes are equipped with absolute divergence dates and all leaf nodes are equipped with sampling dates. Such time-trees have become a central object of study in phylogenetics but little is known about the parameter space of such objects. Here we introduce and study a hierarchy of discrete approximations of the space of time-trees from the graph-theoretic and algorithmic point of view. One of the basic and widely used phylogenetic graphs, the NNI graph, is the roughest approximation and bottom level of our hierarchy. More refined approximations discretize the relative timing of evolutionary divergence and sampling dates. We study basic graph-theoretic questions for these graphs, including the size of neighborhoods, diameter upper and lower bounds, and the problem of finding shortest paths. We settle many of these questions by extending the concept of graph grammars introduced by Sleator, Tarjan, and Thurston to our graphs. Although time values greatly increase the number of possible trees, we show that 1-neighborhood sizes remain linear, allowing for efficient local exploration and construction of these graphs. We also obtain upper bounds on the r-neighborhood sizes of these graphs, including a smaller bound than was previously known for NNI.\n\nOur results open up a number of possible directions for theoretical investigation of graph-theoretic and algorithmic properties of the time-tree graphs. We discuss the directions that are most valuable for phylogenetic applications and give a list of prominent open problems for those applications. In particular, we conjecture that the split theorem applies to shortest paths in time-tree graphs, a property not shared in the general NNI case.

Evolutionary Biology↗

bioRxiv2016

A conditional likelihood is required to estimate the selection coefficient in ancient DNA

Time-series of allele frequencies are a useful and unique set of data to determine the strength of natural selection on the background of genetic drift. Technically, the selection coefficient is estimated by means of a likelihood function built under the hypothesis that the available trajectory spans a sufficiently large portion of the fitness landscape. Especially for ancient DNA, however, often only one single such trajectories is available and the coverage of the fitness landscape is very limited. In fact, one single trajectory is more representative of a process conditioned both in the initial and in the final condition than of a process free to visit the available fitness landscape. Based on two models of population genetics, here we show how to build a likelihood function for the selection coefficient that takes the statistical peculiarity of single trajectories into account. We show that this conditional likelihood delivers a precise estimate of the selection coefficient also when allele frequencies are close to fixation whereas the unconditioned likelihood fails. Finally, we discuss the fact that the traditional, unconditioned likelihood always delivers an answer, which is often unfalsifiable and appears reasonable also when it is not correct.

Evolutionary Biology↗

bioRxiv2016

discoal: flexible coalescent simulations with selection

SummaryHere we describe discoal, a coalescent simulator able to generate population samples that include selective sweeps in a feature-rich, flexible manner. discoal can perform simulations conditioning on the fixation of an allele due to drift or either hard or soft selective sweeps--even those occurring a large genetic distance away from the simulated locus. discoal can simulate sweeps with recurrent mutation to the adaptive allele, recombination, and gene conversion, under nonequilibrium demographic histories and without specifying an allele frequency trajectory in advance.\n\nAvailability and ImplementationAvailability and implementation: discoal is implemented in the C programming language. Source code is freely available on GitHub (https://github.com/kernlab/discoal_multipop) under a GNU General Public License.\n\nContactkern@dls.rutgers.edu\n\nSupplementary informationSupplementary Figures and Text are appended below

Evolutionary Biology↗

bioRxiv2016

Killing by Type VI secretion drives clonal phase separation and the evolution of cooperation

By nature of their small size, dense growth and frequent need for extracellular metabolism, microbes face persistent public goods dilemmas1-5. Spatial assortment can act as a general solution to social conflict by allowing extracellular goods to be utilized preferentially by productive genotypes1,6,7. Established mechanisms that generate microbial assortment depend on the availability of free space8-14; however, microbes often live in densely-packed environments, wherein these mechanisms are ineffective. Here, we describe a novel class of self-organized pattern formation that facilitates the development of spatial structure within densely-packed bacterial colonies. Contact-mediated killing through the Type VI secretion system (T6SS) drives high levels of assortment by precipitating phase separation, even in initially well-mixed populations that do not necessarily exhibit net growth. We examine these dynamics using three different classes of mathematical models and experiments with mutually antagonistic strains of Vibrio cholerae growing on solid media, and find that all appear to de-mix via the same Model A universality class of order-disorder transition. We mathematically demonstrate that contact killing should favour the evolution of public goods cooperation, and empirically examine the relationship between T6SSs and potential cooperation through phylogenetic analysis. Across 26 genera of Proteobacteria and Bacteroidetes, the proportion of a strains genome that codes for potentially-exploitable secreted proteins increases significantly with boththe number of Type 6 secretion systems and the number of T6SS effectors that it possesses. This work demonstrates how antagonistic traits--likely evolved for the purpose of killing competitors--can indirectlylead to the evolution of cooperation by driving genetic phase separation.

Evolutionary Biology↗

bioRxiv2016

Parallel Evolution of Cold Tolerance Within Drosophila melanogaster

Drosophila melanogaster originated in tropical Africa before expanding into strikingly different temperate climates in Eurasia and beyond. Here, we show that elevated cold tolerance has arisen at least three times within this species: beyond the well-studied non-African case, we show that populations from the highlands of Ethiopia and South Africa have significantly increased cold tolerance as well. We observe greater cold tolerance in outbred versus inbred flies, but only in populations with higher inversion frequencies. Each cold-adapted population shows lower inversion frequencies than a closely-related warm-adapted population, suggesting that inversion frequencies may decrease with altitude in addition to latitude. Using the FST-based \"Population Branch Excess\" statistic (PBE), we found only limited evidence for parallel genetic differentiation at the scale of ~4 kb windows, specifically between Ethiopian and South African cold-adapted populations. And yet, when we looked for single nucleotide polymorphisms (SNPs) with codirectional frequency change in two or three cold-adapted populations, strong genomic enrichments were observed from all comparisons. These findings could reflect an important role for selection on standing genetic variation leading to \"soft sweeps\". One SNP showed sufficient codirectional frequency change in all cold-adapted populations to achieve experiment-wide significance: an intronic variant in the synaptic gene Prosap. More generally, proteins involved in neurotransmission were enriched as potential targets of parallel adaptation. The ability to study cold tolerance evolution in a parallel framework will enhance this classic study system for climate adaptation.

Evolutionary Biology↗

bioRxiv2016

Ancient coexistence of norepinephrine, tyramine, and octopamine signaling in bilaterians

Norepinephrine/noradrenaline is a neurotransmitter implicated in arousal and other aspects of vertebrate behavior and physiology. In invertebrates, adrenergic signaling is considered absent and analogous functions are performed by the biogenic amines octopamine and its precursor tyramine. These chemically similar transmitters signal by related families of GPCR in vertebrates and invertebrates, suggesting that octopamine/tyramine are the invertebrate equivalents of vertebrate norepinephrine. However, the evolutionary relationships and origin of these transmitter systems remain unclear. Using phylogenetic analysis and receptor pharmacology, here we establish that norepinephrine, octopamine, and tyramine receptors coexist in some marine invertebrates. In the protostomes Platynereis dumerilii (an annelid) and Priapulus caudatus (a priapulid) we identified and pharmacologically characterized adrenergic 1 and 2 receptors that coexist with octopamine , octopamine {beta}, tyramine type 1, and tyramine 2 receptors. These receptors represent the first examples of adrenergic receptors in protostomes. In the deuterostome Saccoglossus kowalewskii (a hemichordate), we identified and characterized octopamine , octopamine {beta}, tyramine type 1, and tyramine 2 receptors, representing the first example of these receptors in deuterostomes. S. kowalewskii also has adrenergic 1 and 2 receptors, indicating that all three signaling systems coexist in this animal. In phylogenetic analysis, we also identified adrenergic and tyramine receptor orthologs in xenacoelomorphs. Our results clarify the history of monoamine signaling in bilaterians. Since all six receptor families (two each for octopamine and tyramine and three for norepinephrine) can be found in representatives of the two major clades of Bilateria, the protostomes and the deuterostomes, all six receptors coexisted in the protostome-deuterostome last common ancestor. Adrenergic receptors were lost from most insects and nematodes and tyramine and octopamine receptors were lost from most deuterostomes. This complex scenario of differential losses cautions that octopamine signaling in protostomes is not a good model for adrenergic signaling in deuterostomes, and that the studies of marine animals where all three transmitter systems coexist will be needed for a better understanding of the origin and ancestral functions of these transmitters.

Evolutionary Biology↗

bioRxiv2016

Colonization and diversification of aquatic insects on three Macaronesian archipelagos using 59 nuclear loci derived from a draft genome

The study of processes driving diversification requires a fully sampled and well resolved phylogeny. Multilocus approaches to the study of recent diversification provide a powerful means to study the evolutionary process, but their application remains restricted because multiple unlinked loci with suitable variation for phylogenetic or coalescent analysis are not available for most non-model taxa. Here we identify novel, putative single-copy nuclear DNA (nDNA) phylogenetic markers to study the colonization and diversification of an aquatic insect species complex, Cloeon dipterum L. 1761 (Ephemeroptera: Baetidae), in Macaronesia. Whole-genome sequencing data from one member of the species complex were used to identify 59 nDNA loci (32,213 base pairs), followed by Sanger sequencing of 29 individuals sampled from 13 islands of three Macaronesian archipelagos. Multispecies coalescent analyses established six putative species. Three island species formed a monophyletic clade, with one species occurring on the Azores, Europe and North America. Ancestral state reconstruction indicated at least two colonization events from the mainland (Canaries, Azores) and one within the archipelago (between Madeira and the Canaries). Random subsets of the 59 loci showed a positive linear relationship between number of loci and node support. In contrast, node support in the multispecies coalescent tree was negatively correlated with mean number of phylogenetically informative sites per locus, suggesting a complex relationship between tree resolution and marker variability. Our approach highlights the value of combining coalescent-based phylogeography, species delimitation, and phylogenetic reconstruction to resolve recent diversification events in an archipelago species complex.

Evolutionary Biology↗

bioRxiv2016

Single cell transcriptomics, mega-phylogeny and the genetic basis of morphological innovations in Rhizaria

The innovation of the eukaryote cytoskeleton enabled phagocytosis, intracellular transport and cytokinesis, and is responsible for diverse eukaryotic morphologies. Still, the relationship between phenotypic innovations in the cytoskeleton and their underlying genotype is poorly understood. To explore the genetic mechanism of morphological evolution of the eukaryotic cytoskeleton we provide the first single cell transcriptomes from uncultivable, free-living unicellular eukaryotes: the radiolarian species Lithomelissa setosa and Sticholonche zanclea. Analysis of the genetic components of the cytoskeleton and mapping of the evolution of these to a revised phylogeny of Rhizaria reveals lineage-specific gene duplications and neo-functionalization of and {beta} tubulin in Retaria, actin in Retaria and Endomyxa, and Arp2/3 complex genes in Chlorarachniophyta. We show how genetic innovations have shaped cytoskeletal structures in Rhizaria, and how single cell transcriptomics can be applied for resolving deep phylogenies and studying gene evolution of uncultivable protist species.

Evolutionary Biology↗

bioRxiv2016

Nonadaptive Radiation: Pervasive diet specialization by drift in scale insects?

At least half of metazoan species are herbivorous insects. Why are they so diverse? Most herbivorous insects feed on few plant species, and adaptive host specialization is often invoked to explain their diversification. Nevertheless, it is possible that the narrow host ranges of many herbivorous insects are non-adaptive. Here, we test predictions of this hypothesis with comparative phylogenetic analyses of scale insects, a group for which there appears to be few host-use tradeoffs that would select against polyphagy, and for which passive wind-dispersal should make host specificity costly. We infer a strong positive relationship between host range and diversification rate, and a marked asymmetry in cladogenetic changes in diet breadth. These results are consonant with a system of pervasive non-adaptive host specialization in which small, drift- and extinction-prone populations are frequently isolated from persistent and polyphagous source populations. They also contrast with the negative relationship between diet breadth and taxonomic diversification that has been estimated in butterflies, a disparity which likely stems from differences in the average costs and benefits of host specificity and generalism in scale insects vs. butterflies. Our results indicate the potential for non-adaptive processes to be important to diet-breadth evolution and taxonomic diversification across herbivorous insects.

Evolutionary Biology↗

bioRxiv2016

A hidden Markov model approach for simultaneously estimating local ancestry and admixture time using next generation sequence data in samples of arbitrary ploidy

Admixture--the mixing of genomes from divergent populations--is increasingly appreciated as a central process in evolution. To characterize and quantify patterns of admixture across the genome, a number of methods have been developed for local ancestry inference. However, existing approaches have a number of shortcomings. First, all local ancestry inference methods require some prior assumption about the expected ancestry tract lengths. Second, existing methods generally require genotypes, which is not feasible to obtain for many next-generation sequencing projects. Third, many methods assume samples are diploid, however a wide variety of sequencing applications will fail to meet this assumption. To address these issues, we introduce a novel hidden Markov model for estimating local ancestry that models the read pileup data, rather than genotypes, is generalized to arbitrary ploidy, and can estimate the time since admixture during local ancestry inference. We demonstrate that our method can simultaneously estimate the time since admixture and local ancestry with good accuracy, and that it performs well on samples of high ploidy--i.e. 100 or more chromosomes. As this method is very general, we expect it will be useful for local ancestry inference in a wider variety of populations than what previously has been possible. We then applied our method to pooled sequencing data derived from populations of Drosophila melanogaster on an ancestry cline on the east coast of North America. We find that regions of local recombination rates are negatively correlated with the proportion of African ancestry, suggesting that selection against foreign ancestry is the least efficient in low recombination regions. Finally we show that clinal outlier loci are enriched for genes associated with gene regulatory functions, consistent with a role of regulatory evolution in ecological adaptation of admixed D. melanogaster populations. Our results illustrate the potential of local ancestry inference for elucidating fundamental evolutionary processes.\n\nAuthor SummaryWhen divergent populations hybridize, their offspring obtain portions of their genomes from each parent population. Although the average ancestry proportion in each descendant is equal to the proportion of ancestors from each of the ancestral populations, the contribution of each ancestry type is variable across the genome. Estimating local ancestry within admixed individuals is a fundamental goal for evolutionary genetics, and here we develop a method for doing this that circumvents many of the problems associated with existing methods. Briefly, our method can use short read data, rather than genotypes and can be applied to samples with any number of chromosomes. Furthermore, our method simultaneously estimates local ancestry and the number of generations since admixture--the time that the two ancestral populations first encountered each other. Finally, in applying our method to data from an admixture zone between ancestral populations of Drosophila melanogaster, we find many lines of evidence consistent with natural selection operating to against the introduction of foreign ancestry into populations of one predominant ancestry type. Because of the generality of this method, we expect that it will be useful for a wide variety of existing and ongoing research projects.

Evolutionary Biology↗

bioRxiv2016

Theoretical and Empirical Support for Bilateral Decrementation

The concept of \"genetic bandwagoning\" is introduced. In genetic bandwagoning, a bandwagoning allele evaluates the outlook for lineage fitness of the individual holding the allele. If its holders lineage fitness figures to be low, the bandwagoning allele induces its holder to relinquish some, or all, of the holders own resources (e.g., food, territory, mates), which are then used by individuals that happen to be nearby. While some nearby individuals may not possess a copy of the bandwagoning allele, it is likely, if assortment is sufficiently positive, that numerous individuals do and most of those that do have a better lineage fitness outlook than that of the individual that was induced to forfeit the resources, since the inducement is contingent upon a poor lineage fitness outlook. Due to their better lineage fitness outlook, the nearby individuals make better usage of the resources than the forfeiting individuals would have and the ratio between the quantity of descendants nearby individuals produce with the resources and the quantity of descendants that would have been produced by the forfeiting individuals tends to increase with each generation due to multiple reasons examined in section 2. If assortment is sufficiently positive, more copies of the allele are produced over the ensuing generations than if the resources had not been forfeited, as the allele is selected by \"jumping on the bandwagon\" of these fit lineages that use the resources.\n\nTwo ways to bandwagon are introduced: resonation and reservation. In resonation, the bandwagoning allele accomplishes the two steps of bandwagoning--1) evaluating its holders lineage fitness outlook and 2) inducing a holder with a low (i.e., poor) outlook to relinquish resources--sequentially. The necessity for reservation occurs because a lineages fitness outlook can depend upon aspects of quality which are difficult to evaluate during a generation in which many individuals are able to avoid death or serious harm. In reservation, a bandwagoning allele solves this problem of evaluating quality by inducing its holder to reserve from (i.e., withhold) some of its ability to survive against one or more natural enemies, particularly predators or parasites: An individual that can remain healthy in spite of reserving from its ability to survive predators or parasites is likely to have genes that enable its descendants to survive when the predator or parasite threat is more severe; however, if the individual perishes or becomes sick as a result of reservation, its lineage fitness outlook is determined to be low and the relinquishment of resources occurs with this same perishing or sickness. That is, the individuals perishing or sickness due to reservation serves simultaneously: 1) to identify that individual as having a low lineage fitness outlook and 2) as the source of relinquishing the individuals resources on the basis of this low lineage fitness outlook.\n\nGenetic bandwagoning constitutes a novel mechanism for the evolution of cooperation. Numerous paradoxes can be explained by the actions of bandwagoning alleles that use a combination of resonation and reservation, including the phenotypic cooccurrences of robust defenses against parasites and depressive symptoms; phenotypic cooccurrences of robust defenses against parasites and photosynthetic costs; phenotypic cooccurrences of susceptibility to parasites and androgenic benefits; the maintenance of honest signals when there are opportunities to cheat; the forfeiture of reproductive opportunities by functionally capable individuals; and the differential nurturing of offspring.

Evolutionary Biology↗

bioRxiv2016

Towards robust evolutionary inference with integral projection models

Integral projection models (IPMs) are extremely flexible tools for ecological and evolutionary inference. IPMs track the distribution of phenotype in populations through time, using functions describing phenotype-dependent development, inheritance, survival and fecundity. For evolutionary inference, two important features of any model are the ability to (i) characterize relationships among traits (including values of the same traits across ages) within individuals, and (ii) characterize similarity between individuals and their descendants. In IPM analyses, the former depends on regressions of observed trait values at each age on values at the previous age (development functions), and the latter on regressions of offspring values at birth on parent values as adults (inheritance functions). We show analytically that development functions, characterized this way, will typically underestimate covariances of trait values across ages, due to compounding of regression to the mean across projection steps. Similarly, we show that inheritance, characterized this way, is inconsistent with a modern understanding of inheritance, and underestimates the degree to which relatives are phenotypically similar. Additionally, we show that the use of a constant biometric inheritance function, particularly with a constant intercept, is incompatible with evolution. Consequently, current implementations of IPMs will predict little or no phenotypic evolution, purely as artifacts of their construction. We present alternative approaches to constructing development and inheritance functions, based on a quantitative genetic approach, and show analytically and through an empirical example on a population of bighorn sheep how they can potentially recover patterns that are critical to evolutionary inference.

Evolutionary Biology↗

bioRxiv2016

On phylogenetic branch lengths distribution and the late acquistion of mitochondria.

In a recent article, Martin et. al. [1] criticize several methodological aspects of our recent study on the timing of the acquisition of mitochondria [2]. Here we show that our results are independent of the model-based partitioning of the data. In addition, we assess the robustness of our inferences by analyzing data from Martin et. al.

Evolutionary Biology↗

bioRxiv2016

The evolutionary origin of bilaterian smooth and striated myocytes

The dichotomy between smooth and striated myocytes is fundamental for bilaterian musculature, but its evolutionary origin remains unsolved. Given their absence in Drosophila and Caenorhabditis, smooth muscles have so far been considered a vertebrate innovation. Here, we characterize expression profile, ultrastructure, contractility and innervation of the musculature in the marine annelid Platynereis dumerilii and identify smooth muscles around the midgut, hindgut and heart that resemble their vertebrate counterparts in molecular fingerprint, contraction speed, and nervous control. Our data suggest that both visceral smooth and somatic striated myocytes were present in the protostome-deuterostome ancestor, and that smooth myocytes later co-opted the striated contractile module repeatedly - for example in vertebrate heart evolution. During these smooth-to-striated myocyte conversions the core regulatory complex of transcription factors conveying myocyte identity remained unchanged, reflecting a general principle in cell type evolution.

Evolutionary Biology↗

bioRxiv2016

Discovery of flavivirus-derived endogenous viral elements in two Anopheles mosquito genomes supports the existence of Anopheles-associated insect-specific flaviviruses

The Flavivirus genus encompasses several arboviruses of public health significance such as dengue, yellow fever, and Zika viruses. It also includes insect-specific flaviviruses (ISFs) that are only capable of infecting insect hosts. The vast majority of mosquito-infecting flaviviruses have been associated with mosquito species of the Aedes and Culex genera in the Culicinae subfamily, which also includes most arbovirus vectors. Mosquitoes of the Anophelinae subfamily are not considered significant arbovirus vectors, however flaviviruses have occasionally been detected in field-caught Anopheles specimens. Whether such observations reflect occasional spillover or laboratory contamination or whether Anopheles mosquitoes are natural hosts of flaviviruses is unknown. Here, we provide in silico and in vivo evidence of transcriptionally active, flavivirus-derived endogenous viral elements (EVEs) in the genome of Anopheles minimus and Anopheles sinensis. Such non-retroviral endogenization of RNA viruses is consistent with a shared evolutionary history between flaviviruses and Anopheles mosquitoes. Phylogenetic analyses of the two newly described EVEs support the existence of a distinct clade of Anopheles-associated ISFs.

Evolutionary Biology↗

bioRxiv2016

Functional and non-functional classes of peptides produced by long non-coding RNAs

There is accumulating evidence that some genes have originated de novo from previously non-coding genomic sequences. However, the processes underlying de novo gene birth are still enigmatic. In particular, the appearance of a new functional protein seems highly improbable unless there is already a pool of neutrally evolving peptides that can at some point acquire new functions. Here we show for the first time that such peptides do not only exist but that they are prevalent among the translation products of mouse genes that lack homologues in rat and human. The data suggests that the translation of these peptides is due to the chance occurrence of open reading frames with a favorable codon composition. Our approach combines ribosome profiling experiments, proteomics data and non-synonymous and synonymous nucleotide polymorphism analysis. We propose that effectively neutral processes involving the expression of thousands of transcripts all the way down to proteins provide a basis for de novo gene evolution.

Evolutionary Biology↗

bioRxiv2016

Exact calculation of the joint allele frequency spectrum for generalized isolation with migration models

Population genomic datasets collected over the past decade have spurred interest in developing methods that can utilize massive numbers of loci for inference of demographic and selective histories of populations. The allele frequency spectrum (AFS) provides a convenient statistic for such analysis and accordingly much attention has been paid to predicting theoretical expectations of the AFS under a number of different models. However, to date, exact solutions for the joint AFS of two or more populations under models of migration and divergence have not been found. Here we present a novel Markov chain representation of the coalescent on the state space of the joint AFS that allows for rapid, exact calculation of the joint AFS under isolation with migration (IM) models. In turn, we show how our Markov chain method, in the context of composite likelihood estimation, can be used for accurate inference of parameters of the IM model using SNP data. Lastly, we apply our method to recent whole genome datasets from African Drosophila melanogaster.

Evolutionary Biology↗