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bioRxiv2020

Evolutionary feedbacks between genes and their extended effects under limited gene flow and biased ecological inheritance

Organisms continuously modify their living conditions via extended genetic effects on their envi-ronment, microbiome, and in some species culture. These effects can impact the fitness of current but also future conspecifics due to non-genetic transmission via ecological or cultural inheritance. In this case, selection on a gene with extended effects depends on the degree to which current and future genetic relatives are exposed to modified conditions. Here, we detail the selection gradient on a quantitative trait with extended effects in a patch-structured population, when gene flow between patches is limited and ecological inheritance within patches can be biased towards offspring. Such a situation is relevant to understand evolutionary driven changes in individual condition that can be preferentially transmitted from parent to offspring, such as cellular state, micro-environments (e.g., nests), pathogens, microbiome, or culture. Our analysis quantifies how the interaction between limited gene flow and biased ecological inheritance influences the joint evolutionary dynamics of traits together with the conditions they modify, helping understand adaptation via non-genetic modifications. As an illustration, we apply our analysis to a gene-culture coevolution scenario in which genetically-determined learning strategies coevolve with adaptive knowledge. In particular, we show that when social learning is synergistic, selection can favour strategies that generate remarkable levels of knowledge under intermediate levels of both vertical cultural transmission and limited dispersal. More broadly, our theory yields insights into the interplay between genetic and non-genetic inheritance, with implications for how organisms evolve to transform their environments.

evolutionary biology↗

bioRxiv2020

Scientometric correlates of high-quality reference lists in ecological papers

It is said that the quality of a scientific publication is as good as the science it cites, but the properties of high-quality reference lists have never been numerically quantified. We examined seven numerical characteristics of reference lists of 50,878 primary research articles published in 17 ecological journals between 1997 and 2017. Over this 20-years period, there have been significant changes in reference lists’ properties. On average, more recent ecological papers have longer reference lists, cite more high Impact Factor papers, and fewer non-journal publications. Furthermore, we show that highly cited papers across the ecology literature have longer reference lists, cite more recent and impactful papers, and account for more self-citations. Conversely, the proportion of ‘classic’ papers and non-journal publications cited, as well as the temporal range of the reference list, have no significant influence on articles’ citations. From this analysis, we distill a recipe for crafting impactful reference lists.View Full Text

scientific communication and education↗

bioRxiv2020

Ecological and social drivers of neighbor recognition and the dear enemy effect in a poison frog

Navigating social relationships frequently rests on the ability to recognize familiar individuals using phenotypic characteristics. Across diverse taxa, animals vary in their capacities for social recognition but the ecological and social sources of selection for recognition are often unclear. In a comparative study of two closely related species of poison frogs, we identified a species difference in social recognition of territory neighbors and investigated potential sources of selection underlying this difference. In response to acoustic playbacks, male golden rocket frogs (Anomaloglossus beebei) recognized the calls of neighbors and displayed a "dear enemy effect" by responding less aggressively to neighbors calls than strangers calls. In contrast, male Kai rocket frogs (Anomaloglossus kaiei) were equally aggressive to the calls of neighbors and strangers. This species difference in behavior was associated with key differences in reproductive ecology and characteristics of territories. Golden rocket frogs defended reproductive resources in the form of bromeliads, which is expected to create a threat asymmetry between neighbors and strangers favoring decreased aggression to neighbors. In contrast, Kai rocket frogs did not defend reproductive resources. Further, compared with Kai rocket frog territories, golden rocket frog territories occurred at higher densities and were defended for longer periods of time, creating a more complex social environment with more opportunities for repeated but unnecessary aggression between neighbors, which should favor the ability to recognize and exhibit less aggression towards neighbors. These results suggest that differences in reproductive ecology can drive changes in social structure that select for social recognition.

animal behavior and cognition↗

bioRxiv2020

Cooperation increases robustness to ecological disturbance in microbial cross-feeding networks

Microorganisms mainly exist within complex networks of ecological interactions. Given that the growth and survival of community members frequently depend on an obligate exchange of essential metabolites, it is generally unclear how such communities can persist despite the destabilizing force of ecological disturbance. Here we address this issue using a population dynamics model. In contrast to previous work that suggests the potential for obligate interaction networks to evolve is limited, we find the opposite pattern: natural selection in the form of ecological disturbance favors both specific network topologies and cooperative cross-feeding among community members. These results establish environmental selection as a key driver shaping the architecture of microbial interaction networks.

evolutionary biology↗

bioRxiv2020

Genus-wide characterization of bumblebee genomes reveals variation associated with key ecological and behavioral traits of pollinators

Bumblebees are a diverse group of globally important pollinators in natural ecosystems and for agricultural food production. With both eusocial and solitary lifecycle phases, and some social parasite species, they are especially interesting models to understand social evolution, behavior, and ecology. Reports of many species in decline point to pathogen transmission, habitat loss, pesticide usage, and global climate change, as interconnected causes. These threats to bumblebee diversity make our reliance on a handful of well-studied species for agricultural pollination particularly precarious. To broadly sample bumblebee genomic and phenotypic diversity, we de novo sequenced and assembled the genomes of 17 species, representing all 15 subgenera, producing the first genus-wide quantification of genetic and genomic variation potentially underlying key ecological and behavioral traits. The species phylogeny resolves subgenera relationships while incomplete lineage sorting likely drives high levels of gene tree discordance. Five chromosome-level assemblies show a stable 18-chromosome karyotype, with major rearrangements creating 25 chromosomes in social parasites. Differential transposable element activity drives changes in genome sizes, with putative domestications of repetitive sequences influencing gene coding and regulatory potential. Dynamically evolving gene families and signatures of positive selection point to genus-wide variation in processes linked to foraging, diet and metabolism, immunity and detoxification, as well as adaptations for life at high altitudes. These high-quality genomic resources capture natural genetic and phenotypic variation across bumblebees, offering new opportunities to advance our understanding of their remarkable ecological success and to identify and manage current and future threats.

genomics↗

bioRxiv2020

A chromosome-level genome assembly for the Eastern Fence Lizard (Sceloporus undulatus), a reptile model for physiological and evolutionary ecology

High-quality genomic resources facilitate population-level and species-level comparisons to answer questions about behavioral ecology, morphological and physiological adaptations, as well as the evolution of genomic architecture. Squamate reptiles (lizards and snakes) are particularly diverse in characteristics that have intrigued evolutionary biologists, but high-quality genomic resources for squamates are relatively sparse. Lizards in the genus Sceloporus have a long history as important ecological, evolutionary, and physiological models, making them a valuable target for the development of genomic resources. We present a high-quality chromosome-level reference genome assembly, SceUnd1.0, (utilizing 10X Genomics Chromium, HiC, and PacBio data) and tissue/developmental stage transcriptomes for the Eastern Fence Lizard, Sceloporus undulatus. We performed synteny analysis with other available squamate chromosome-level assemblies to identify broad patterns of chromosome evolution including the fusion of micro- and macrochromosomes in S. undulatus. Using this new S. undulatus genome assembly we conducted reference-based assemblies for 34 other Sceloporus species to improve draft nuclear genomes assemblies from 1% coverage to 43% coverage on average. Across these species, typically >90% of reads mapped for species within 20 million years divergence from S. undulatus, this dropped to 75% reads mapped for species at 35 million years divergence. Finally we use RNAseq and whole genome resequencing data to compare the three assemblies as references, each representing an increased level of sequencing, cost and assembly efforts: Supernova Assembly with data from10X Genomics Chromium library; HiRise Assembly that added data from HiC library; and PBJelly Assembly that added data from PacBio sequencing. We found that the Supernova Assembly contained the full genome and was a suitable reference for RNAseq, but the chromosome-level scaffolds provided by the addition of the HiC data allowed the reference to be used for other whole genome analysis, including synteny and whole genome association mapping analyses. The addition of PacBio data provided negligible gains. Overall, these new genomic resources provide valuable tools for advanced molecular analysis of an organism that has become a model in physiology and evolutionary ecology.

genomics↗

bioRxiv2020

Ecological Specialization and Diversification in Birds

Ecological specialization is widely thought to influence patterns of species richness by affecting rates at which species multiply and perish. Quantifying specialization is challenging, and using only one or a small number of ecological axes could bias estimates of overall specialization. Here, we calculate an index of specialization, based on seven measured traits, and estimate its effect on speciation and extinction rates in a large clade of birds. We find that speciation rate is independent of specialization, suggesting independence of local ecology and the geographic distributions of populations that promote allopatric species formation. Although some analyses suggest that more specialized species have higher extinction rates, leading to negative net diversification, this relationship is not consistently identified across our analyses. Our results suggest that specialization may drive diversification dynamics only on local scales or in specific clades, but is not generally responsible for macroevolutionary disparity in lineage diversification rates.

evolutionary biology↗

bioRxiv2020

Ecological specialization promotes diversity and diversification in the East Mediterranean genus Ricotia (Brassicaceae)

Despite its amazing biodiversity, the Eastern Mediterranean remains a highly understudied region especially when compared to the Western Mediterranean. Scarcity of such studies restrict our understanding of the processes shaping diversity across the entire Mediterranean. To this end we used a combination of molecular markers and presence/absence data from all species of the Eastern Mediterrranean genus Ricotia collected across its full geographic range to determine historical, ecological and evolutionary factors responsible for lineage-specific diversification in this genus. Network analysis based on nuclear ribosomal and chloroplast DNA revealed high genetic structure within all lineages and phylogenetic reconstructions based on the multispecies coalescent showed that within lineage diversification corresponded to the onset of the Mediterranean climate. Reconstruction of ancestral histories indicate the genus originated within Anatolia and slowly spread across the Eastern Mediterranean and Levant using the Taurus mountains. Ecological niche models based on climatic and environmental variables suggest local populations did not go through any major distributional shifts and have persisted in present day habitats since the LGM. Furthermore, niche differentiation tests revealed significant niche differences between closely related species and showed the main variables predicting species limits to be different for each species. Our results give crucial information on the patterns and processes shaping diversity in the Eastern Mediterranean and show the main factor promoting diversification to be local environmental dynamics and ecological specialization and not large scale latitudinal movements as often reported for southern Europe. By determining regional and global patterns of diversification in an eastern Mediterranean genus we further our understanding of the major trends influencing plant diversity in the Mediterranean basin as a whole.

evolutionary biology↗

bioRxiv2020

Urbanization alters ecological and evolutionary interaction between Darwin's Finches and Tribulus cistoides on the Galapagos Islands

Emerging evidence suggests that urbanization shapes the ecology and evolution of species interactions. Islands are particularly susceptible to urbanization due to the fragility of their ecosystems; however, few studies have examined the effects of urbanization on species interactions on islands. To address this gap, we studied the effects of urbanization on interactions between Darwins finches and its key food resource, Tribulus cistoides, in three towns on the Galapagos Islands. We assessed the effects of urbanization on seed and mericarp removal, mericarp morphology, and finch community composition using natural population surveys, experimental manipulations, and finch observations. We found that both seed and fruit removal rates were higher in urban compared to non-urban populations in the natural and experimental populations, and that urbanization modified selection on mericarp size and defense. Urban environments supported smaller and less diverse finch communities than non-urban environments. Together, our results suggest that urbanization can dramatically alter ecological interactions between Darwins finches and T. cistoides, leading to modified selection on T. cistoides populations. Our study demonstrates that urban development on islands can have profound effects on the ecology and evolution of trophic interactions.

evolutionary biology↗

bioRxiv2020

Costly mate preferences can promote reproductive isolation along ecological gradients

Species often replace each other spatially along contact zones, giving scope for parapatric speciation. In models of parapatric speciation driven by assortative mating, costs of female choosiness have so far be ignored. Yet, if females encounter only a limited number of males, those that are too choosy may remain unmated, and this should create direct sexual selection against choosiness. In our individual-based model of parapatric ecological speciation, disruptive viability selection leads to divergence of an ecological trait. Additionally, female choosiness (following a matching mating rule based on the same ecological trait) can evolve at the risk of remaining unmated, and can limit gene flow between diverging populations. In line with previous litterature, out of the contact zone, the evolution of cost-free choosiness stops at intermediate values due to indirect selection against strong choosiness. Here we show that a weak cost of choosiness, by modifying genotypic frequencies on which viability selection acts, reduces this selection pressure, thus permitting the evolution of stronger choosiness than in the absence of costs. In strong contrast to sympatric models, costs of choosiness can therefore promote reproductive isolation in parapatry.

evolutionary biology↗

bioRxiv2020

Inhibitory control, personality, and manipulated ecological conditions influence foraging plasticity in the great tit

O_LIOrganisms are consistently under selection to respond effectively to a diversity of, sometimes rapid, changes in their environment. Behavioural plasticity can allow individuals to do so instantaneously, but why individuals vary in this respect is poorly understood. Although personality and cognitive traits are often hypothesised to influence plasticity, the effects reported are highly inconsistent, which we hypothesise is because ecological context is usually not considered. C_LIO_LIHere we explore the roles of individual cognitive and personality variation - assayed using standard tasks for inhibitory control, a measure of self-control, and reactive-proactive personality axis (RPPA), respectively - in driving foraging plasticity, and asked how these effects varied across two experimentally manipulated ecological contexts: food value and predation risk. C_LIO_LIAfter great tits (Parus major) had initially been trained to retrieve high value food hidden in sand, they were then simultaneously offered the hidden food and an alternative food choice on the surface, that was either high or low value. Their choices were further examined under high and low perceived predation risk treatments. Individuals choices were classified in terms of whether they continued to forage on the hidden but familiar food source, or instead switched to the new visible food source. We defined the latter option as the plastic response. C_LIO_LIOur assays captured consistent differences among individuals in foraging behaviour. Both inhibitory control and exploration influenced whether birds switched from the familiar but hidden food source to the new alternative visible food on the surface. These effects depended on the relative value of the food items available and on the perceived level of predation risk, but also on the time scale over which the response was measured. C_LIO_LIOur results demonstrate how an executive cognitive function and one specific personality axis can simultaneously influence plasticity in a key functional behaviour. That their effects on foraging were primarily observed as interactions with food value or predation risk treatments also suggest that the population level consequences of behavioural mechanisms, such as these, may only be revealed across key ecological conditions or gradients. C_LI

animal behavior and cognition↗

bioRxiv2021

Phylogeny of the damselfishes (Pomacentridae) and patterns of asymmetrical diversification in body size and feeding ecology

The damselfishes (family Pomacentridae) inhabit near-shore communities in tropical and temperature oceans as one of the major lineages in coral reef fish assemblages. Our understanding of their evolutionary ecology, morphology and function has often been advanced by increasingly detailed and accurate molecular phylogenies. Here we present the next stage of multi-locus, molecular phylogenetics for the group based on analysis of 12 nuclear and mitochondrial gene sequences from 345 of the 422 damselfishes. The resulting well-resolved phylogeny helps to address several important questions about higher-level damselfish relationships, their evolutionary history and patterns of divergence. A time-calibrated phylogenetic tree yields a root age for the family of 55.5 mya, refines the age of origin for a number of diverse genera, and shows that ecological changes during the Eocene-Oligocene transition provided opportunities for damselfish diversification. We explored the idea that body size extremes have evolved repeatedly among the Pomacentridae, and demonstrate that large and small body sizes have evolved independently at least 40 times and with asymmetric rates of transition among size classes. We tested the hypothesis that transitions among dietary ecotypes (benthic herbivory, pelagic planktivory and intermediate omnivory) are asymmetric, with higher transition rates from intermediate omnivory to either planktivory or herbivory. Using multistate hidden-state speciation and extinction models, we found that both body size and dietary ecotype are significantly associated with patterns of diversification across the damselfishes, and that the highest rates of net diversification are associated with medium body size and pelagic planktivory. We also conclude that the pattern of evolutionary diversification in feeding ecology, with frequent and asymmetrical transitions between feeding ecotypes, is largely restricted to the subfamily Pomacentrinae in the Indo-West Pacific. Trait diversification patterns for damselfishes across a fully resolved phylogeny challenge many recent general conclusions about the evolution of reef fishes.

evolutionary biology↗

bioRxiv2021

Reevaluating claims of ecological speciation in Halichoeres bivittatus

Understanding the role of ecological processes in speciation has become one of the most active areas of research in marine population biology in recent decades. The traditional view was that allopatry was the primary driver of speciation in marine taxa, but the geography of the marine environment and the dispersal capabilities of many marine organisms render this view somewhat questionable. One of the earliest and most highly cited empirical examples of ecological speciation with gene flow in marine fishes is that of the slippery dick wrasse, Halichoeres bivittatus. Evidence for this cryptic or incipient speciation event was primarily in the form of a deep north-south divergence in a single mitochondrial locus, combined with a finding that these two haplotypes were associated with different habitat types in the Florida Keys and Bermuda, where they overlap. Here we examine habitat assortment in the Florida Keys using a broader sampling of populations and habitat types than were available for the original study, and find no evidence to support the claim that haplotype frequencies differ between habitat types, and little evidence to support any differences between populations. These results severely undermine claims of ecological speciation with gene flow in Halichoeres bivittatus. We argue that future claims of this type should be supported by multiple lines of evidence that illuminate potential mechanisms and allow researchers to rule out alternative explanations for spatial patterns of genetic differences.

evolutionary biology↗

bioRxiv2021

Ecological correlates of gene family size: the draft genome of the redheaded pine sawfly Neodiprion lecontei

A central goal in evolutionary biology is to determine the predictability of adaptive genetic changes. Despite many documented cases of convergent evolution at individual loci, little is known about the repeatability of gene family expansions and contractions. To address this void, we examined gene family evolution in the redheaded pine sawfly Neodiprion lecontei, a non-eusocial hymenopteran and exemplar of a pine-specialized lineage evolved from angiosperm-feeding ancestors. After assembling and annotating a draft genome, we manually annotated multiple gene families with chemosensory, detoxification, or immunity functions and characterized their genomic distributions and evolutionary history. Our results suggest that expansions of bitter gustatory receptor (GR), clan 3 cytochrome P450 (CYP3), and antimicrobial peptide (AMP) subfamilies may have contributed to pine adaptation. By contrast, there was no evidence of recent gene family contraction via pseudogenization. Next, we compared the number of genes in these same families across insect taxa that vary in diet, dietary specialization, and social behavior. In Hymenoptera, herbivory was associated with small GR and olfactory receptor (OR) families, eusociality was associated with large OR and small AMP families, and--unlike investigations in more closely related taxa--ecological specialization was not related to gene family size. Overall, our results suggest that gene families that mediate ecological interactions may expand and contract predictably in response to particular selection pressures, however, the ecological drivers and temporal pace of gene gain and loss likely varies considerably across gene families.

evolutionary biology↗

bioRxiv2021

EMBED: a low dimensional reconstruction of gut microbiome dynamics based on ecological normal modes

Dimensionality reduction can offer unique insights into high dimensional microbiome dynamics by leveraging collective abundance fluctuations of multiple bacteria driven by similar ecological perturbations. However, methods providing lower-dimensional representations of microbiome dynamics both at the community and individual taxa level are not currently available. To that end, we present EMBED: Essential MicroBiomE Dynamics, a probabilistic non-linear tensor factorization approach. Similar to normal mode analysis in structural biophysics, EMBED infers ecological normal modes (ECNs), which represent the unique orthogonal modes capturing the collective behavior of microbial communities. A very small number of ECNs can accurately approximate microbiome dynamics across multiple data sets. Inferred ECNs reflect specific ecological behaviors, providing natural templates along which the dynamics of individual bacteria may be partitioned. Moreover, the multi-subject treatment in EMBED systematically identifies subject-specific and universal abundance dynamics that are not detected by traditional approaches. Collectively, these results highlight the utility of EMBED as a versatile dimensionality reduction tool for studies of microbiome dynamics.

systems biology↗

bioRxiv2021

Mutation rate dynamics reflect ecological changes in an emerging zoonotic pathogen

While mutation is often deleterious, it can also be adaptive. Mutation rates vary both within and between bacterial species, and understanding what drives this variation is essential for understanding the evolutionary dynamics of bacterial populations. In this study we investigate two factors that are predicted to influence the trade-off between the costs and benefits of mutation: ecology and genome size. To investigate the relationship between these factors and mutation rate we conducted mutation accumulation experiments on eight strains of the emerging zoonotic pathogen Streptococcus suis. Natural variation within this species allows us to compare tonsil carriage and invasive disease isolates, from both more and less pathogenic populations, with a wide range of genome sizes. We find that invasive disease isolates have repeatedly evolved mutation rates that are higher than those of closely related carriage isolates, regardless of variation in genome size. Independent of this variation in overall rate, we also observe a stronger bias towards G/C to A/T mutations in isolates from more pathogenic populations, whose genomes tend to be smaller and more AT-rich. Our results suggest that ecology is a stronger correlate of mutation rate than genome size over these timescales, and that transitions to invasive disease are consistently accompanied by rapid increases in mutation rate. These results shed light on the impact ecology can have on the adaptive potential of bacterial pathogens.

evolutionary biology↗

bioRxiv2021

Punctual ecological changes rather than global factors drive species diversification and the evolution of wing phenotypes in Morpho butterflies.

Assessing the relative importance of geographical and ecological drivers of evolution is paramount to understand the diversification of species and traits at the macroevolutionary scale. Here, we use an integrative approach, combining phylogenetics, biogeography, ecology, and quantified phenotypes to investigate the drivers of both species and phenotypic diversification of the iconic Neotropical butterfly genus Morpho. We generated a time-calibrated phylogeny for all known species and inferred historical biogeography. We fitted models of time-dependent (accounting for rate heterogeneity across the phylogeny) and paleoenvironment-dependent diversification (accounting for global effect on the phylogeny). We used geometric morphometrics to assess variation of wing size and shape across the tree, and investigated their dynamics of evolution. We found that the diversification of Morpho is best explained when considering multiple independent diversification dynamics across the tree, possibly associated with lineages occupying different microhabitat conditions. First, a shift from understory to canopy was characterized by an increased speciation rate partially coupled with an increasing rate of wing shape evolution. Second, the occupation of dense bamboo thickets accompanying a major host-plant shift from dicotyledons towards monocotyledons was associated with a simultaneous diversification rate shift and an evolutionary "jump" of wing size. Our study points to a diversification pattern driven by punctual ecological changes instead of a global driver or biogeographic history.

evolutionary biology↗

bioRxiv2021

Plasmid co-infection: linking biological mechanisms to ecological and evolutionary dynamics

As infectious agents of bacteria and vehicles of horizontal gene transfer, plasmids play a key role in bacterial ecology and evolution. Plasmid dynamics are shaped not only by plasmid-host interactions, but also by ecological interactions between plasmid variants. These interactions are complex: plasmids can co-infect the same host cell and the consequences for the co-resident plasmid can be either beneficial or detrimental. Many of the biological processes that govern plasmid co-infection-from systems to exclude infection by other plasmids to interactions in the regulation of plasmid copy number per cell-are well characterised at a mechanistic level. Modelling plays a central role in translating such mechanistic insights into predictions about plasmid dynamics, and in turn, the impact of these dynamics on bacterial evolution. Theoretical work in evolutionary epidemiology has shown that formulating models of co-infection is not trivial, as some modelling choices can introduce unintended ecological assumptions. Here, we review how the biological processes that govern co-infection can be represented in a mathematical model, discuss potential modelling pitfalls, and analyse this model to provide general insights into how co-infection impacts eco-evolutionary outcomes. In particular, we demonstrate how beneficial and detrimental effects of co-infection give rise to frequency-dependent selection.

microbiology↗