Biology subjects

Kocher, S. D.

Publications and source records attributed to Kocher, S. D..

16 recordsLinked to original sources

bioRxiv2025

The distribution of fitness effects varies phylogenetically across animals

1The distribution of fitness effects (DFE) describes the selection coefficients (s) of newly arising mutations and fundamentally influences population genetic processes. However, the extent and mechanisms of DFE variation have not been systematically investigated across species with divergent phylogenetic histories and ecological functions. Here, we inferred the DFE in natural populations of eleven animal (sub)species, including humans, mice, fin whales, vaquitas, wolves, collared flycatchers, pied flycatchers, halictid bees, Drosophila, and mosquitoes. We find that the DFE co-varies with phylogeny, where the expected mutation effects are more similar in closely related species (Pagels{lambda} = 0.84, P = 0.01). Additionally, mammals have a higher proportion of strongly deleterious mutations (22% to 47% in mammals; 0.0% to 5.4% in insects and birds) and a lower proportion of weakly deleterious mutations than insects and birds. Population size is significantly negatively correlated with the expected impact of new deleterious mutations (PGLS{lambda}, P = 0.03), and the proportion of new beneficial mutations ([Formula], P < 0.001). These findings align with Fishers Geometric Model (FGM), which defines organismal complexity as the number of phenotypes under selection. Consistent with the FGMs predictions, we observe that mutations are more deleterious in complex organisms, while beneficial mutations occur more frequently in smaller populations to compensate for the drift load. Our study demonstrates strong phylogenetic constraints in the evolution of a fundamental population genetics parameter, and proposes that, through mechanisms of global epistasis, long-term population size and organismal complexity drive variation in the DFE across animals. 2 Significance StatementUnderstanding how mutations affect fitness is fundamental in evolution, but little is known about how and why the distribution of fitness effects (DFE) varies across species. In this study, we examine the DFE in diverse animal populations and show that closely related species exhibit similar patterns of mutation effects, with new mutations being more deleterious in mammals compared with birds and insects. Our findings corroborate Fishers Geometric Model, which explains the variation in the DFE across species as a function of organismal complexity and long-term population size. By connecting organismal complexity and population size with the DFE, we offer a phylogenetic view into the selective forces shaping species adaptation and evolution.

evolutionary biology↗

bioRxiv2025

The fire ant social chromosome exerts a major influence on genome regulation

Supergenes underlying complex trait polymorphisms ensure sets of coadapted alleles remain genetically linked. Despite their prevalence in nature, the mechanisms of supergene effects on genome regulation are poorly understood. In the fire ant Solenopsis invicta, a supergene containing over 500 individual genes influences trait variation in multiple castes to collectively underpin a colony level social polymorphism. Here, we present results of an integrative investigation of supergene effects on gene regulation. We present analyses of ATAC-seq data to investigate variation in chromatin accessibility by supergene genotype and STARR-seq data to characterize enhancer activity by supergene haplotype. Integration with gene coexpression analyses, newly mapped intact TEs, and previously identified CNVs, collectively reveal widespread effects of the supergene on chromatin structure, gene transcription, and regulatory element activity, with a genome-wide bias for open chromatin and increased expression in the presence of the derived supergene haplotype, particularly in regions that harbor intact TEs. Integrated consideration of CNVs and regulatory element divergence suggests each evolved in concert to shape the expression of supergene encoded factors, including several transcription factors that may directly contribute to the trans-regulatory footprint of a heteromorphic social chromosome. Overall, we show how genome structure in the form of a supergene has wide-reaching effects on gene regulation and gene expression.

genomics↗

bioRxiv2025

Queen loss unmasks cryptic worker influence and decentralizes the bumble bee social network

Dominant individuals often structure group organization, but less is known about how social networks reorganize in their absence and how variation among subordinates contributes to collective outcomes. Bumble bees (Bombus impatiens) provide an ideal system to study these dynamics: queens typically monopolize reproduction, but in some contexts individual workers can adopt queenlike social roles. Using multi-animal pose tracking, we compared matched queenright and queenless partitions from the same source colonies, quantifying over 80 million social interactions. Queen-less colonies exhibited increased behavioral variation and contained a subset of highly influential workers with elevated movement, spatial centrality, and reproductive activity that was absent in queen-right conditions. The emergence of these individuals coincided with a shift from centralized to decentralized, efficient network architectures. These results demonstrate that queen presence constrains latent worker variation, revealing how individual behavioral differences can scale up to reshape collective social organization in hierarchical societies.

animal behavior and cognition↗

bioRxiv2024

pipemake: A pipeline creation tool using Snakemake for reproducible analysis of biological datasets

The exponential growth in biological data generation has created an urgent need for efficient, reproducible computational analysis workflows. Here, we present pipemake, a computational platform designed to streamline the development and implementation of efficient and reproducible Snakemake workflows. pipemake creates modular pipelines that can be seamlessly integrated or removed from the platform without requiring reconfiguration of the core system, enabling flexible adaptation of workflows to different analytical needs across diverse fields. To demonstrate the platforms capabilities, we created and implemented pipelines to reanalyze two distinct biological datasets. First, we recreated a population genomics analysis of the socially flexible halictid bee, Lasioglossum albipes, using pipemake-generated workflows for de novo genome annotation, processing of variant data, dimensionality reduction, and a genome-wide association study (GWAS). We then used pipemake to analyze behavioral tracking data from the common eastern bumble bee, Bombus impatiens. In both cases, pipemake workflows produced results consistent with published findings while substantially reducing hands-on analysis time. Overall, pipemakes modular design allows researchers to easily modify existing pipelines or develop new ones without software development expertise. Beyond streamlining workflow creation, pipemake leverages the full Snakemake ecosystem to enable parallel processing, automated error recovery, and comprehensive analysis documentation. These features make pipemake an efficient and accessible solution for analyzing complex biological datasets. pipemake is freely available as a conda package or direct download at https://github.com/kocherlab/pipemake

bioinformatics↗

bioRxiv2024

Repeated shifts in sociality are associated with fine-tuning of highly conserved and lineage-specific enhancers in a socially flexible bee

Comparative genomic studies of social insects suggest that changes in gene regulation are associated with evolutionary transitions in social behavior, but the activity of predicted regulatory regions has not been tested empirically. We used STARR-seq, a high-throughput enhancer discovery tool, to identify and measure the activity of enhancers in the socially variable sweat bee, Lasioglossum albipes. We identified over 36,000 enhancers in the L. albipes genome from three social and three solitary populations. Many enhancers were identified in only a subset of L. albipes populations, revealing rapid divergence in regulatory regions within this species. Population-specific enhancers were often proximal to the same genes across populations, suggesting compensatory gains and losses of regulatory regions may preserve gene activity. We also identified 1182 enhancers with significant differences in activity between social and solitary populations, some of which are conserved regulatory regions across species of bees. These results indicate that social trait variation in L. albipes is driven both by the fine-tuning of ancient enhancers as well as lineage-specific regulatory changes. Combining enhancer activity with population genetic data revealed variants associated with differences in enhancer activity and identified a subset of differential enhancers with signatures of selection associated with social behavior. Together, these results provide the first empirical map of enhancers in a socially flexible bee and highlight links between cis-regulatory variation and the evolution of social behavior.

evolutionary biology↗

bioRxiv2024

Chromosomal fusion drives sex chromosome evolution in treehoppers despite long-term X chromosome conservation

Sex chromosomes follow distinct evolutionary trajectories compared to the rest of the genome. In many cases, sex chromosomes (X and Y, or Z and W) significantly differentiate from one another resulting in heteromorphic sex chromosome systems. Such heteromorphic systems are thought to act as an evolutionary trap that prevents subsequent turnover of the sex chromosome system. For old, degenerated sex chromosome systems in which turnover is unlikely, chromosomal fusion with an autosome may be one way that sex chromosomes can refresh their sequence content. We investigated these dynamics using treehoppers (hemipteran insects of the family Membracidae), which ancestrally have XX/X0 sex chromosomes. We assembled the first chromosome-level treehopper genome from Umbonia crassicornis and employed comparative genomic analyses of 12 additional treehopper species to analyze X chromosome variation across different evolutionary timescales. We find that the X chromosome is largely conserved, with one exception being an X-autosome fusion in Calloconophora caliginosa. We also compare the ancestral treehopper X with other X chromosomes in Auchenorrhyncha (the clade containing treehoppers, leafhoppers, spittlebugs, cicadas, and planthoppers), revealing X conservation across more than 300 million years. These findings shed light on chromosomal evolution dynamics in treehoppers and the role of chromosomal rearrangements in sex chromosome evolution. SignificanceThe evolutionary forces underlying sex chromosome stability versus turnover have been challenging to disentangle. We present the first chromosome-level treehopper genome and find evidence of long-term X chromosome conservation within treehoppers - and among treehoppers and other hemipteran insects. A key exception is the evolution of neo-XX/XY sex chromosomes via an X-autosome fusion. Sex chromosome-autosome fusions may play an important role in the evolution of otherwise trapped (i.e., old and degenerated) sex chromosome systems.

evolutionary biology↗

bioRxiv2024

Variation in season length and development time is sufficient to drive the emergence and coexistence of social and solitary behavioral strategies

Season length and its associated variables can influence the expression of social behaviors, including the occurrence of eusociality in insects. Eusociality can vary widely across environmental gradients, both within and between different species. Numerous theoretical models have been developed to examine the life history traits that underlie the emergence and maintenance of eusociality, yet the impact of seasonality on this process is largely uncharacterized. Here, we present a theoretical model that incorporates season length and offspring development time into a single, individual-focused model to examine how these factors can shape the costs and benefits of social living. We find that longer season lengths and faster brood development times are sufficient to favor the emergence and maintenance of a social strategy, while shorter seasons favor a solitary one. We also identify a range of season lengths where social and solitary strategies can coexist. Moreover, our theoretical predictions are well-matched to the natural history and behavior of two flexibly-eusocial bee species, suggesting our model can make realistic predictions about the evolution of different social strategies. Broadly, this work reveals the crucial role that environmental conditions can have in shaping social behavior and its evolution and underscores the need for further models that explicitly incorporate such variation to study evolutionary trajectories of eusociality.

evolutionary biology↗

bioRxiv2023

Developmental transcriptomes predict adult social behaviors in the socially flexible sweat bee, Lasioglossum baleicum

Natural variation can provide important insights into the genetic and environmental factors that shape social behavior and its evolution. The sweat bee, Lasioglossum baleicum, is a socially flexible bee capable of producing both solitary and eusocial nests. We demonstrate that within a single nesting aggregation, soil temperatures are a strong predictor of the social structure of nests. Sites with warmer temperatures in the spring have a higher frequency of social nests than cooler sites, perhaps because warmer temperatures provide a longer reproductive window for those nests. To identify the molecular correlates of this behavioral variation, we generated a de novo genome assembly for L. baleicum, and we used transcriptomic profiling to compare adults and developing offspring from eusocial and solitary nests. We find that adult, reproductive females have similar expression profiles regardless of social structure in the nest, but that there are strong differences between reproductive females and workers from social nests. We also find substantial differences in the transcriptomic profiles of stage-matched pupae from warmer, social-biased sites compared to cooler, solitary-biased sites. These transcriptional differences are strongly predictive of adult reproductive state, suggesting that the developmental environment may set the stage for adult behaviors in L. baleicum. Together, our results help to characterize the molecular mechanisms shaping variation in social behavior and highlight a potential role of environmental tuning during development as a factor shaping adult behavior and physiology in this socially flexible bee.

genomics↗

bioRxiv2022

NAPS: Integrating pose estimation and tag-based tracking

O_LISignificant advances in computational ethology have allowed the quantification of behavior in unprecedented detail. Tracking animals in social groups, however, remains challenging as most existing methods can either capture pose or robustly retain individual identity over time but not both. C_LIO_LITo capture finely resolved behaviors while maintaining individual identity, we built NAPS (NAPS is ArUco Plus SLEAP), a hybrid tracking framework that combines state-of-the-art, deep learning-based methods for pose estimation (SLEAP) with unique markers for identity persistence (ArUco). We show that this framework allows the exploration of the social dynamics of the common eastern bumblebee (Bombus impatiens). C_LIO_LIWe provide a stand-alone Python package for implementing this framework along with detailed documentation to allow for easy utilization and expansion. We show that NAPS can scale to long timescale experiments at a high frame rate and that it enables the investigation of detailed behavioral variation within individuals in a group. C_LIO_LIExpanding the toolkit for capturing the constituent behaviors of social groups is essential for understanding the structure and dynamics of social networks. NAPS provides a key tool for capturing these behaviors and can provide critical data for understanding how individual variation influences collective dynamics. C_LI

animal behavior and cognition↗

bioRxiv2022

Hormonal gatekeeping via the blood brain barrier governs behavior

Here we reveal an unanticipated role of the blood-brain-barrier (BBB) in regulating complex social behavior in ants. Using scRNA-seq we find localization in the BBB of a key hormone-degrading enzyme called Juvenile hormone esterase (Jhe), and we show that this localization governs the level of Juvenile Hormone (JH3) entering the brain. Manipulation of the Jhe level reprograms the brain transcriptome between ant castes. While ant Jhe is retained and functions intracellularly within the BBB, we show that Drosophila Jhe is naturally extracellular. Heterologous expression of ant Jhe into the Drosophila BBB alters behavior in fly to mimic what is seen in ant. Most strikingly, manipulation of Jhe levels in ant reprograms complex behavior between worker castes. Our study thus uncovers a novel, potentially conserved role of the BBB serving as a molecular gatekeeper for a neurohormonal pathway that regulates social behavior.

neuroscience↗

bioRxiv2021

Isolation disrupts social interactions and destabilizes brain development in bumblebees

Social isolation, particularly in early life, leads to deleterious physiological and behavioral outcomes. Few studies, if any, have been able to capture the behavioral and neurogenomic consequences of early life social isolation together in a single social animal system. Here, we leverage new high-throughput tools to comprehensively investigate the impact of isolation in the bumblebee (Bombus impatiens) from behavioral, molecular, and neuroanatomical perspectives. We reared newly emerged bumblebees either in complete isolation, small groups, or in their natal colony, and then analyzed their behaviors while alone or paired with another bee. We find that when alone, individuals of each rearing condition show distinct behavioral signatures. When paired with a conspecific, bees reared in small groups or in the natal colony express similar behavioral profiles. Isolated bees, however, showed increased social interactions. To identify the neurobiological correlates of these differences, we quantified brain gene expression and measured the volumes of key brain regions for a subset of individuals from each rearing condition. Overall, we find that isolation increases social interactions and disrupts gene expression and brain development. Limited social experience in small groups is sufficient to preserve typical patterns of brain development and social behavior.

animal behavior and cognition↗

bioRxiv2021

Convergent selection on juvenile hormone signaling is associated with the evolution of eusociality in bees

Sweat bees have repeatedly gained and lost eusociality, a transition from individual to group reproduction. Here, we generate chromosome-length genome assemblies for 17 species and identify genomic signatures of evolutionary trade-offs associated with transitions between social and solitary living. Both young genes and regulatory regions show enrichment for these molecular patterns. We also identify loci that show evidence of complementary signals of positive and relaxed selection linked specifically to the convergent gains and losses of eusociality in sweat bees. This includes two proteins that bind and transport juvenile hormone (JH) - a key regulator of insect development and reproduction. We find one of these JH binding proteins is primarily expressed in subperineurial glial cells that form the insect blood-brain barrier and that brain levels of JH vary by sociality. Our findings are consistent with a role of JH in modulating social behavior and suggest eusocial evolution was facilitated by alteration of the proteins that bind and transport JH, revealing how an ancestral, developmental hormone may have been co-opted during one of lifes major transitions. More broadly, our results highlight how trade-offs have structured the molecular basis of eusociality in these bees and demonstrate how both directional selection and release from constraint can shape trait evolution.

evolutionary biology↗

bioRxiv2020

SLEAP: Multi-animal pose tracking

The desire to understand how the brain generates and patterns behavior has driven rapid methodological innovation to quantify and model natural animal behavior. This has led to important advances in deep learning-based markerless pose estimation that have been enabled in part by the success of deep learning for computer vision applications. Here we present SLEAP (Social LEAP Estimates Animal Poses), a framework for multi-animal pose tracking via deep learning. This system is capable of simultaneously tracking any number of animals during social interactions and across a variety of experimental conditions. SLEAP implements several complementary approaches for dealing with the problems inherent in moving from single-to multi-animal pose tracking, including configurable neural network architectures, inference techniques, and tracking algorithms, enabling easy specialization and tuning for particular experimental conditions or performance requirements. We report results on multiple datasets of socially interacting animals (flies, bees, and mice) and describe how dataset-specific properties can be leveraged to determine the best configuration of SLEAP models. Using a high accuracy model (<2.8 px error on 95% of points), we were able to track two animals from full size 1024 x 1024 pixel frames at up to 320 FPS. The SLEAP framework comes with a sophisticated graphical user interface, multi-platform support, Colab-based GPU-free training and inference, and complete tutorials available, in addition to the datasets, at sleap.ai.

animal behavior and cognition↗

bioRxiv2018

Rate variation in conserved noncoding DNA reveals regulatory pathways associated with social evolution

The evolutionary origins of eusociality represent increases in complexity from individual to caste-based, group reproduction. These behavioral transitions have been hypothesized to go hand-in-hand with an increased ability to regulate when and where genes are expressed. Bees have convergently evolved eusociality up to five times, providing a framework to test this hypothesis. To examine potential links between putative gene regulatory elements and social evolution, we compare alignable, non-coding sequences in eleven diverse bee species, encompassing three independent origins of reproductive division of labor and two elaborations of eusocial complexity. We find that rates of evolution in a number of non-coding sequences correlate with key social transitions in bees. Interestingly, while we find little evidence for convergent rate changes associated with independent origins of social behavior, a number of molecular pathways exhibit convergent rate changes in conjunction with subsequent elaborations of social organization. We also present evidence that many novel non-coding regions may have been recruited alongside the origin of sociality in corbiculate bees; these loci could represent gene regulatory elements associated with division of labor within this group. Thus, our findings are consistent with the hypothesis that gene regulatory innovations are associated with the evolution of eusociality and illustrate how a thorough examination of both coding and non-coding sequence can provide a more complete understanding of the molecular mechanisms underlying behavioral evolution.

evolutionary biology↗

bioRxiv2018

Investigating the viral ecology of global bee communities with high-throughput metagenomics

Bee viral ecology is a fascinating emerging area of research: viruses exert a range of effects on their hosts, exacerbate the impacts of other environmental stressors, and, importantly, are readily shared across multiple bee species in a community. However, our understanding of bee viral communities is limited, as it is primarily derived from studies of North American and European Apis mellifera populations. Here, we examined viruses in populations of A. mellifera and 11 other bee species from 9 countries, across 5 continents and Oceania. We developed a novel pipeline to rapidly, inexpensively, and robustly screen for bee viruses. This pipeline includes purification of encapsulated RNA/DNA viruses, sequence-independent amplification, high throughput sequencing, integrated assembly of contigs, and filtering to identify contigs specifically corresponding to viral sequences. We identified sequences corresponding to (+)ssRNA, (-)ssRNA, dsRNA, and ssDNA viruses. Overall, we found 127 contigs corresponding to novel viruses (i.e. previously not observed in bees), with 29 represented by >0.1 % of the reads in a given sample. These viruses and viral families were distributed across multiple regions and species. This study provides a robust pipeline for metagenomics analysis of viruses, and greatly expands our understanding of the diversity of viruses found in bee communities.

genomics↗

bioRxiv2017

Social behavior in bees influences the abundance of Sodalis (Enterobacteriaceae) symbionts

Social interactions can facilitate transmission of microbes between individuals, reducing variation in gut communities within social groups. Thus, the evolution of social behaviors and symbiont community composition have the potential to be tightly linked. We explored this connection by characterizing the diversity of bacteria associated with both social and solitary bee species within the behaviorally variable family Halictidae using 16S amplicon sequencing. Contrary to expectations, we found few differences in bacterial abundance or variation between social forms, and most halictid species appear to share similar gut bacterial communities. However, several strains of Sodalis, a genus described as a symbiont in a variety of insects but yet to be characterized in bees, differ in abundance between social and solitary bees. Phylogenetic reconstructions based on whole-genome alignments indicate that Sodalis has independently colonized halictids at least three times. These strains appear to be mutually exclusive within individual bees, although they are not host-species-specific and no signatures of vertical transmission were observed, suggesting that Sodalis strains compete for access to hosts. De novo genome assemblies indicate that these three lineages are subject to widespread relaxed selection and that Sodalis is undergoing genome degeneration during the colonization of these hosts.

microbiology↗