Caste-biased gene expression in a facultatively eusocial bee suggests a role for genetic accommodation in the evolution of eusociality

Jones, Beryl M.; Kingwell, Callum J.; Wcislo, William T.; Robinson, Gene E.

doi:10.1098/rspb.2016.2228

Cited by 44 publications

(72 citation statements)

References 69 publications

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“…Most of these studies have either focused on brain or whole body samples 15,22,24,26,33,[35][36][37] , although expression bias between queens and workers has been shown to be dependent upon developmental stage and tissue type 34,[38][39][40] . Finally, the transcriptomic signatures of reproductive physiology are strongest in the abdomen 34,41 , the location of reproductive organs, but no past study has explicitly compared caste bias in abdominal tissues in species from lineages representing independent origins of eusociality.…”

Section: Introductionmentioning

confidence: 99%

Convergent eusocial evolution is based on a shared reproductive groundplan plus lineage-specific plastic genes

Warner

Qiu

Holmes

et al. 2018

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Eusociality has convergently evolved multiple times, but the genomic basis of caste-based division of labor and degree to which independent origins of eusociality have utilized common genes remain largely unknown. Here we characterize caste-specific transcriptomic profiles across development and adult body segments from pharaoh ants (Monomorium pharaonis) and honey bees (Apis mellifera), representing two independent origins of eusociality. We identify a substantial shared core of genes upregulated in the abdomens of queen ants and honey bees that also tends to be upregulated in mated female flies, suggesting that these genes are part of a conserved insect reproductive groundplan. Outside of this shared groundplan, few genes are differentially expressed in common. Instead, the majority of the thousands of caste-associated genes are plastically-expressed, rapidly evolving, and relatively evolutionarily young. These results emphasize that the recruitment of both highly conserved and lineage-specific genes underlie the convergent evolution of novel traits such as eusociality.

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Section: Introductionmentioning

confidence: 99%

Convergent eusocial evolution is based on a shared reproductive groundplan plus lineage-specific plastic genes

Warner

Qiu

Holmes

et al. 2018

Preprint

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“…As such, caste traits are not fixed during development, and females who served as non-reproductive workers can become reproductive queens if given the opportunity [69]. This flexibility is reflected in the magnitude of differences in brain gene expression patterns between queen and worker honey bees (thousands of genes [48]) and M. genalis (dozens of genes [40]). Previous research suggests that miRNAs increase their functional influence over evolutionary time [10,11,65,66,70,71].…”

Section: Discussionmentioning

confidence: 99%

“…The complete list of included studies and gene lists are in Table S4. For M. genalis caste data, RNAseq reads from Jones et al [40] (NCBI PRJNA331103) were trimmed using Trimmomatic (v. 0.36) [41] and aligned to an unpublished genome assembly of M. genalis (NCBI PRJNA494872) using STAR (v. 2.5.3) [42]. Reads were mapped to gene features using featureCounts in the Subread package (v. 1.5.2) [43].…”

Section: Methodsmentioning

confidence: 99%

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Brain microRNAs among social and solitary bees

Kapheim

Jones

Søvik

et al. 2019

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37Evolutionary transitions to a social lifestyle in insects are associated with lineage-specific 38 changes in gene expression, but the key nodes that drive these regulatory changes are largely 39 unknown. We tested the hypothesis that changes in gene regulation associated with social 40 evolution are facilitated by lineage-specific function of microRNAs (miRNAs). Genome scans 41 across 12 bee species showed that miRNA copy-number is mostly conserved and not associated 42 with sociality. However, deep sequencing of small RNAs in six bee species revealed a 43 substantial proportion (20-35%) of detected miRNAs had lineage-specific expression in the 44 brain, 24-72% of which did not have homologs in other species. Lineage-specific miRNAs 45 disproportionately target lineage-specific genes, and have lower expression levels than shared 46 miRNAs. The predicted targets of lineage-specific miRNAs are enriched for genes related to 47 social behavior in social species, but they are not enriched for genes under positive selection. 48Together, these results suggest that novel miRNAs may contribute to lineage-specific patterns of 49 social evolution. Our analyses also support the hypothesis that many new miRNAs are purged by 50 selection due to deleterious effects on mRNA targets, and suggest genome structure is not as 51 influential in regulating bee miRNA evolution as has been shown for mammalian miRNAs. 52 53 specific 55 56 57Eusociality has evolved several times in the hymenopteran insects. In its most basic form, 58 this lifestyle involves reproductive queens living with their worker daughters who forego direct 59 reproduction to cooperatively defend the nest, care for their siblings, and forage for the colony. 60 Due to the complex nature of this lifestyle, the evolution of eusociality likely requires 61 modification of molecular pathways related to development, behavior, neurobiology, physiology, 62 and morphology [1]. The evolution of eusociality is thus expected to involve both genetic 63 changes as well as changes in the way the genome responds to the environment [2]. It is 64therefore unsurprising that recent studies aimed at identifying the genomic signatures of eusocial 65 evolution in insects have found that social species share an increased capacity for gene regulation 66 [3,4]. Evidence for this comes from signatures of rapid evolution of genes involved in 67 transcription and translation, gene family expansions of transcription factors, and increasing 68 potential for DNA methylation and transcription factor binding activity in conserved genes. 69Interestingly, while these types of regulatory changes are common to independent origins and 70 elaborations of eusociality, the specific genes and regulatory elements involved are unique to 71 each lineage [3][4][5]. This suggests that lineage-specific processes are influential in generating new 72 patterns of gene regulation that contribute to social behavior. 73 74 Small, non-coding RNAs such as microRNAs (miRNAs) may be an important source of 75 regulatory novel...

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“…This means that just as changes in gene expression drive cell type specifications, they should also drive developmentally-determined caste differentiation in the social insects. There is growing evidence to support this assertion, including well-documented changes in gene expression in developing larvae and in adults [12][13][14][15][16][17][18][19][20][21][22], as well as changes in DNA methylation [23][24][25][26], post-translational histone modifications, and chromatin accessibility [27][28][29].…”

Section: Introductionmentioning

confidence: 99%

Rate variation in the evolution of non-coding DNA associated with social evolution in bees

Jones

Hunt

et al. 2018

Preprint

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14The evolutionary origins of eusociality represent increases in complexity from individual to caste-15 based, group reproduction. These behavioral transitions have been hypothesized to go hand-in- 16hand with an increased ability to regulate when and where genes are expressed. Bees have 17 convergently evolved eusociality up to five times, providing a framework to test this hypothesis. 18To examine potential links between putative gene regulatory elements and social evolution, we 19 compare alignable, non-coding sequences in eleven diverse bee species, encompassing three 20 independent origins of reproductive division of labor and two elaborations of eusocial complexity. 21We find that rates of evolution in a number of non-coding sequences correlate with key social 22 transitions in bees. Interestingly, while we find little evidence for convergent rate changes 23 associated with independent origins of social behavior, a number of molecular pathways exhibit 24 convergent rate changes in conjunction with subsequent elaborations of social organization. We 25 also present evidence that many novel non-coding regions may have been recruited alongside 26 the origin of sociality in corbiculate bees; these loci could represent gene regulatory elements 27 associated with division of labor within this group. Thus, our findings are consistent with the 28 hypothesis that gene regulatory innovations are associated with the evolution of eusociality and 29 illustrate how a thorough examination of both coding and non-coding sequence can provide a 30 more complete understanding of the molecular mechanisms underlying behavioral evolution. 32 33Introduction 34 35Many genomic sequences that do not encode proteins play essential roles in gene regulation 36 across animals [1] and plants [2]. The breadth of knowledge of these non-coding regulatory 37 elements has been built primarily upon the large number of plant and vertebrate genomes that 38 have been sequenced over the past decade. However, the high degree of conservation that exists 39 in a subset of these non-coding regions [1,3] means that comparative methods can be used to 40 identify similar non-coding elements even in the recently sequenced genomes of non-model taxa 41 that frequently lack the resources needed to characterize regulatory regions via functional assays. outside of Drosophila [4], the non-coding regulatory landscape of these taxa has been the target 44 of few studies. 46Here, we take advantage of eleven publicly-available bee genomes [5][6][7][8][9] to examine how non-47 coding elements change as eusociality -an extreme form of social behavior found primarily in 48 insects and mammals -has convergently evolved and increased in complexity within bees. 49Eusociality is of particular interest to evolutionary biologists because it represents an increase in 50 complexity from individual to group-level reproduction and includes the evolution of a non-51 reproductive worker caste [10]. Along with reproductively-specialized castes, many of these 52 societies have also e...

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Caste-biased gene expression in a facultatively eusocial bee suggests a role for genetic accommodation in the evolution of eusociality

Cited by 44 publications

References 69 publications

Convergent eusocial evolution is based on a shared reproductive groundplan plus lineage-specific plastic genes

Convergent eusocial evolution is based on a shared reproductive groundplan plus lineage-specific plastic genes

Brain microRNAs among social and solitary bees

Rate variation in the evolution of non-coding DNA associated with social evolution in bees

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