How do castes evolve in eusocial species?

How do castes evolve in eusocial species?

We are searching data for your request:

Forums and discussions:
Manuals and reference books:
Data from registers:
Wait the end of the search in all databases.
Upon completion, a link will appear to access the found materials.

I have been reading about eusocial species and have some questions. What is the basis for caste differentiation? Is it entirely genetic? Does the queen have the code for soldiers, workers etc in her own genes, so only a mutation to the queen results in change of the whole colony's castes? As a related question, how do different castes evolve?

It seems to me that if only one individual in a colony is reproducing, the rate of evolution must necessarily be much slower because any genetic change in the queen would affect all castes, which is likely to have some negative effects.

Does a fertile queen have the code for soldiers/workers in its own genes, so only a mutation to the queen results in change of the whole coloniy's castes?


But how that would protect them from just going extinct due to one unfavorable mutation to a queen?

One unfavorable mutation to a queen could make that queen and her lineage "extinct". It wouldn't necessarily have any effect on the rest of the population (i.e. other queens and their lineages). There's no difference here between eusocial and other species.

Ants are eusocial and close relatives of bees and wasps. Ant and bees use Haplodiploidy. it is a sex-determination system in which males develop from unfertilized eggs and are haploid, and females develop from fertilized eggs and are diploid.

Young queen ants leaving the nest can have one or 10 or 20 fathers. The new queens and workers are not necessarilly clones, and defective genes can be omitted in workers and queens.

the queen may be inseminated by more than 15-20 males, it's polygynous, versus mono androus (andros being male in greek).

Some queens can mate with different species of ant and hybridize.

A nuptial flight of 10 queens in the first year and 1000 queens in the 10th year, all those individuals will have different genetics, because they all come from different fertilized eggs. The males are drones and all the same.

It can vary by species of ant, the queens can be all the same: in the ant Cataglyphis cursor, the queens are produced by parthenogenesis but workers arise from fertilized eggs, suggesting that genetic variation is vital for the worker caste (Pearcy et al. 2004).

Here is an attempt to unify the literature on ant caste development and evolution with a single theoretical framework, drawing on recent advances in evolutionary developmental biology.

They say that ant populations contain a balance little to big ants, a range of sizes, whereby queen like features, ovaries, wings and light receptors between teh eyes called ocelli, appear in steps as the larvae grow. Ants molt and the develop from small workers to large queens progressively.

If you check an soldier ant, she has a large head, it's almost as big as a queen's, although the body stays small. in the next stage of caste size, the body grows into nearly a queen, else with wings too.

If there is a lack of one caste, more of a particular kind are replenished.

To read the paper faster, search for keywords, for example hormones, they say:

Two endocrine hormones, juvenile hormone (JH) and ecdysone, are important regulators of developmental timing in insects. Pupation (and the cessation of larval growth) is triggered by ecdysone, and the action of ecdysone is inhibited by JH (Hiruma and Kaneko, 2013). Thus, treatment of larvae with JH or JH analogs leads to prolonged growth and larger size, as long as necessary nutrition is present. JH removal and/or ecdysone treatment leads to premature pupation and smaller adult size (Hiruma and Kaneko, 2013). This endocrine regulation of insect size has been demonstrated in Coleoptera and Lepidoptera, and is also supported by experiments in ants.

Some of the small ants have the potential to become queens, and when there is lots of food, more of the small ones will grow and make many queens that can fly on a hot day.

In M. rubra, larvae do not have the potential for queen development under normal conditions (Brian, 1979). However, larvae that are forced to diapause just before pupation reorganize their endocrine organs and delay pupation after growth is resumed (Brian, 1979). If sufficient nutrition is available, these totipotent larvae attain a large size and develop into queens

You may laugh by reading the effective genetic ant population mathematics at the end of the first citation. it is completely professor level, with a maths formula, which demonstrates that it's extraordinarily complex and variable effective genetic population distribution and gene expression.

If someone can say more about eusocial gene determination it's quite a difficult topic.

Eusocial Insect Evolution

Eusociality generally affords a great survival advantage to any group of animals, and is likely best exemplified in insects. Behavioral characteristics include the cooperative care of offspring, distinct castes of workers (often sterile) that do not sexually reproduce and groups that do, and well defined divisions of labor. The behaviors of distinct groups are genetically coded, and one caste has lost the ability to perform functions of other castes. Eusociality is highly refined and abundant in insect Order Hymenoptera (the ants, bees and wasps), as well as in Infraorder Isoptera, Order Blattodea (the termites). There are also eusocial, aphids, and thrips. However, there is considerable differentiation between species in extent and type of eusocial behavior. Among the hymenopterans, ants are far and away the most social (almost all species), most having highly refined labor division, and have even been noted for collective colonial problem solving. Bees and wasps as a group are far less social, with some highly social lineages, and other lineages having entirely solitary behavior. The Isopterans are highly eusocial, where a single king and queen perform all reproduction, and there are castes of workers and soldiers.

Darwin's Problem and the Genetic Basis of Eusocial Traits

The high prevalence of eusociality among hymenopterans compared to its general rarity within the animal kingdom has been an area of debate in evolutionary biology, and the new genomics sequencing technologies are enabling its study in detail. In a simple view of Darwinian evolution, such altruistic self-sacrificing of one’s own genes could be viewed as contradictory. But, according to Hughes (et al., 2008), eusociality evolved eight to ten times within Hymenoptera. In The Origin of Species, Darwin described sterile worker castes in the social insects as "the one special difficulty, which at first appeared to me insuperable and actually fatal to my whole theory". The dilemma has been explained by the concept of “inclusive fitness” a combination of individual reproductive success and reproductive success of a group having similar genes. In simple mathematical terms, the portion of the altruist’s genes that are passed on exceeds those that would be passed on in an individual effort to procreate. We now know it’s more complex than this due to females having diploid cells (having two homologous copies of each chromosome, one from each parent), and males having haploid cells (with but one chromosome). Consequently, males share only 25% of their sisters' genes, whereas females on average share 50% of their sister's genes, which is the same as it would be with their own offspring. Evolution will select for altruistic cooperation when it's more efficient to raise siblings than offspring, providing a sustainable selective advantage of eusociality because the collective expends less energy per offspring by its cooperative behaviors and division of labor. The relatedness of sisters diminishes should the queen not be sexually monogamous. Interestingly, many ants, bees, and wasps have evolved behavior of lifetime monogamy, where the queen mates with one and only one male, who dies afterwards. This monogamous trait is an ancestral characteristic in all eusocial Hymenopteran lineages (Hughes, 2008).

Basic Natural Selection in Evolution of Eusocial Altruism

The above explains the genetic basis for eusocial behavior being maintained in a lineage, but how did it arise? That would be fairly straightforward natural selection. First, some advantage was accrued by common nesting, and selected for. Mutations and selection led to selective silencing of genes for individual wandering (e.g., loss in wings in worker castes). Behavior beneficial to the queen’s reproduction is reinforced. Finally, colonial lineages that are eusocial outcompete those that are not.

Recent Evolutionary Biology Studies of Eusocial Behavior, Enter Sociogenomics



Reproductive mode in which unfertilized eggs develop into haploid males and fertilized eggs develop into diploid females.

Cooperative behavior among individuals of the same species characterized by reproductive division of labor, overlap of generations, and cooperative nesting.

Insects characterized by complete metamorphosis, a wingless larval stage, and an intermediate pupal stage.

A parasitoid that develops on a paralyzed, incapacitated host.

A parasitoid that develops on a mobile, active host.

A group in which all species are descended from a single common ancestor and all descendants of the ancestor are classified in the group characterized by shared derived characters.

Modified appendages of the seventh and eighth abdominal segments used for egg laying.

A group in which only some of the species descended from an ancestor are classified together characterized by shared ancestral characters.

An organism in which the immature stage feeds and develops on a single host arthropod, resulting in the death of the host.

Reproduction in which eggs are not fertilized by males.

Branching pattern of evolutionary relationships among organisms.

Reproductive mode in which unfertilized eggs develop into diploid females.

How could an eusocial dragon species of elemental castes work?

Well here are constant questions about how control, breath or thrown different "elemental" objects, electricity, fire, ice, water, air and the less common earth (because requieres things like gravity control) all of these trying to be the most realistic possible, usually asked in terms of "dragons", like the classic fire breathing dragon (even the napalm thrower) or the ligthning thrower dragon (or just electric contact), the crygenic dragon or the wind dragon.

Then eusocial animals normally have castes or a very marked work division with different characteristics between members of the same specie, ants for example have workers, soldiers, drones and a queen, almost the same with termites, bees and wasps and a notorious example at fiction are the xenomorph from alien.

So, gonna let it in terms of dragons for practical reasons (but still open the option of ant-like creatures or other animal), thinking about a specie of eusocial dragons which have a queen which produce different castes that obviously have differences of size and other less notorious characteristics but the most interesting feature is that each of this castes could breath a different "element" (based on the mentioned dragons).

I know almost nothing about the evolution of eusocial animals with these very different castes, since they are different from what I know of sexual selection, so therefore I do not know how these anatomical differences between the castes are produced from a single queen and for this case with the "dragons" it is more difficult to know if all these breaths could arise from something like a more basic and primitive organ structure.

The only things that I know about this kind of animals is that comes from animals that originally were not social and was convergent in many different animals, so till where I know the polimorphic variations of the castes are caused for the same reasons which produce "races", for a specie with a high genetical variability in this case brought to the extreme and combined with posterior polifenism changes caused by the enviroment.

Then I could concluse that for get this eusocial "elemental" creature is required start with a specie in which just the individual variations produce the very different "breathings". But I am nor sure if this breathing structures can be developed after the "eusocialization" as a subproduct of this.

So, maybe the primordial structures that the queen should have for produce the other castes can be limited to just three, because according to what I read they can be used as precursors to others because changing or adding some things can have multiple functions. These are:

  • Electric, because can be used as lighter for develop lightning, fire or napalm.
  • Napalm or other substance, because have the "container" for create the required substances for be throwing.
  • Cryogenic, is the mores strange, but probably change the orientiation, can chane from "ice" to "heat" or to air currents.

Of curse how I mentioned these structures can be developed after the eusocialization but for this case I do not have options.

Finally for mention the ideas for the castes:

  • The bigger soldiers being fire breather.
  • The workers, could be ice or cryogenic breathers for build some structures (but maybe this need a big "refrigerator" body), the other option a sticky substance like napalm could work.
  • Light drones, maybe would be electric or even ligthning throwers.
  • And I already mentioned the options for the queen.

Many other characteristics can be added but that could push even more the limits of the polimorphism, so we will be atenied to a very similar body format with just size varitions but with this different "breathings".

So, I am asking what process would permit a queen having all breath types to create individuals with individual breath types?

Also there are a lot of more dragons or thrower animals that I did not want include because if I dont the principals less I know that, but I am gonna let those here for reference.


November 10th, 2020

Understanding the evolution of eusociality, defined by distinct reproductive and nonreproductive castes, at the molecular level, has always been an essential and highly challenging topic of biology. Eusociality has evolved multiple times independently and involved many incremental steps, resulted in intermediate levels of social complexity. The Apinae (corbiculate bees) consists of 4 tribes with a wide range of social complexity: orchid bees (Euglossini), bumble bees (Bombini), stingless bees (Meliponini), and honey bees (Apini) is an ideal group for comparative studies of eusocial evolution in Hymenoptera. The first sequenced genome of the honey bee Apis mellifera in 2006 has become a gateway for numerous studies of corbiculate bees. However, most studies focused on only a relatively small taxa number and a narrow range of social lifestyle, which leads to a knowledge gap that has hindered our ability to understand what happens at the molecular level during this major evolutionary transition.

Previous studies revealed several exceptional traits of the Apini species genome, including a low but heterogeneous GC content with a bimodal distribution, the highest recombination rate among the metazoan. Because eusociality and high recombination rates may co-evolve, we suspect that the advanced eusocial lifestyle does contribute to the Apis mellifera GC content bimodality. Based on our current base compositional analysis on various Hymenoptera insects, we have found evidence that the bimodal GC content distribution is profound in the Apini tribe bees and is not a universal trait of eusociality. We hypothesize these differences in genomic base composition are associated with the social complexity level and evolution of eusociality in corbiculate bees. Therefore, this project’s main objective is to elucidate the evolutionary forces that shape genomic base composition in the eusocial corbiculate bees genome. We are proposing to accomplish this goal with the following aims: 1) Investigate the mutation of corbiculate bees and gain better insight into the mutation rate between different social level bees 2) Estimate the recombination rate of eusocial corbiculate bees 3) Resolve the origin of advanced eusociality in corbiculate bees.

Materials and methods

Source material

P. canadensis wasps of known behavioral repertoires were collected from wild populations in Panama, in July 2009 (Punta Galeta, Colon). All wasps were collected directly off their nests with forceps around midday during the active periods (that is, sunny weather) and preserved immediately in RNAlater (Ambion, Invitrogen, Applied Biosystems), and stored at -20°C until analysis (Section 1 in Additional file 1).

Transcriptome sequencing, assembly and analyses

454 sequencing of pooled samples of 37 wasps across phenotypes (5 to 18 individuals per phenotype 2.1 million reads, 80% brain, 10% abdomen, and 10% antennae) was used to generate a reference transcriptome (Section 2 in Additional file 1). Newbler v2.3 was used to generate the final assembled gene set (Table S1 in Additional file 1). Transcripts were annotated using GO categories assigned using BLASTx of GenBank NR databases with a conservative e-value threshold of 10 -5 , and Blast2Go was used to assess enrichment of GO terms among phenotypes (Section 4 in Additional file 1). Illumina sequencing of 14 biological replicates (>377 million reads) across 5 lanes was conducted to quantify differential gene expression, expressed as RPKM (reads per kilobase per million) values (Section 8 in Additional file 1). We trialed a number of methods for identifying differentially expressed genes and settled on a novel non-parametric method (NOISeq [59]) This method infers the noise distribution from the data and performs pairwise comparison of the samples to identify differentially expressed genes. A variety of probability thresholds were tested (Section 8 in Additional file 1). For the GO analysis we used a q-value >0.6 that represents a 50% chance that the gene is differentially expressed rather than not differentially expressed.

Phylogenetic analyses

Protein sequences were aligned using MUSCLE [72], with default parameters. This is a multiple sequence aligner that includes an iterative alignment refinement phase to overcome known pitfalls of the progressive alignment strategy. Subsequently, poorly aligned regions of the alignment were trimmed with trimAl v1.3. [73] to remove columns with gaps in more than 30% of the sequences. A maximum-likelihood analysis was conducted on the concatenated alignment containing 33,506 sites using PhyML v3.0 [74]. Out of a total of five evolutionary models (LG, JTT, WAG, VT, BLOSUM62), the general replacement model LG (after 'Lee and Gascuel') was found to be the best fitting model using the AIC criterion [75]. In all cases four categories of evolutionary rates were used, estimating the gamma shape parameter and the proportion of invariable sites from the data. Branch supports were obtained using an approximate likelihood ratio test as implemented in PhyML ('Minimum of SH and chi-square' option). The resulting topology was compared to an alternative topology placing Polistes as a sister group to the ants. To do so, the phylogeny was re-computed, fixing the monophyly of Polistes and ants, but allowing the rest of the topology to be optimized. Support for the two topologies were compared using a Shimodaira-Hasegawa test, as implemented in CONSEL [76]. A Bayesian analysis was conducted as implemented in PhyloBayes [77], using the default CAT model and running two independent MCMC runs during 300,000 generations, and sampling every 100 generations. Consensus trees were built after removing the first 20% sampled trees and using a majority consensus rule.

Data access

Raw sequence data are available at the European Read Archive (accession number ERP001342). The Transcriptome Shotgun Assembly project has been deposited at DDBJ/EMBL/GenBank under the accession GAFR01000001-GAFR01045087. The version described in this paper is the first version, GAFR01000000. All data and datasets can also be accessed at [78].

Robinson, G. E., Grozinger, C. M. & Whitfield, C. W. Sociogenomics: social life in molecular terms. Nat. Rev. Genet. 6, 257–270 (2005).

Rehan, S. M. & Toth, A. L. Climbing the social ladder: the molecular evolution of sociality. Trends Ecol. Evolution 30, 426–433 (2015).

West-Eberhard, M. J Developmental Plasticity and Evolution.(Oxford University Press: 2003.

Kapheim, K. M. et al. Genomic signatures of evolutionary transitions from solitary to group living. Science 348, 1139–1143 (2015).

Simola, D. F. et al. Social insect genomes exhibits dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality. Genome Res. 23, 1235–1247 (2013).

Rubinstein, D. R. et al. Coevolution of genome architecture and social behavior. Trends Ecol. Evolution 34, 844–855 (2019).

Michener, C. D. Comparative social behavior of bees. Annu. Rev. Entomol. 14, 299–342 (1969).

Wilson, E. O The Insect Societies. (Belknap Press of Harvard University Press: 1971.

Cardinal, S. & Danforth, B. N. The antiquity and evolutionary history of social behavior in bees. PLOS ONE 6, e21086 (2011).

Gibbs, J., Brady, S. G., Kanda, K. & Danforth, B. N. Phylogeny of halictine bees supports a shared origin of eusociality for Halictus and Lasioglossum (Apoidea: Anthophila: Halictidae). Mol. Phylogenet. Evol. 65, 926–939 (2012).

Rehan, S. M., Leys, R. & Schwarz, M. P. A mid-Cretaceous origin of sociality in Xylocopine bees with only two origins of true worker castes indicates severe barriers to eusociality. PLoS ONE 7, e34690 (2012).

Szathmary, E. & Smith, J. M. The major evolutionary transitions. Nature 374, 227–232 (1995).

Michener, C. D The Bees of the World. 2nd edn., ((Johns Hopkins University Press: 2007.

West-Eberhard, M. J. in Natural History and Evolution of Paper Wasps (eds Turillazzi, S., West-Eberhard, M.J.) 291–317 (Oxford University Press, 1996).

Gadagkar, R. The evolution of caste polymorphism in social insects: genetic release followed by diversifying evolution. J. Genet. 76, 167–179 (1997).

Wilson, E. O. & Hölldobler, B. Eusociality: origin and consequences. Proc. Natl Acad. Sci. USA 102, 13367–13371 (2005).

Schwarz, M. P., Tierney, S. M., Rehan, S. M., Chenoweth, L. B. & Cooper, S. J. B. The evolution of eusociality in allodapine bees: workers began by waiting. Biol. Lett. 7, 277–280 (2011).

Toth, A. L. & Robinson, G. E. Evo-devo and the evolution of social behavior. Trends Genet. 23, 334–341 (2007).

Toth, A. L. & Rehan, S. M. Molecular evolution of insect sociality: an eco-evo-devo perspective. Annu. Rev. Entomol. 62, 419–442 (2017).

Mikát, M., Franchino, C. & Rehan, S. M. Sociodemographic variation in foraging behavior and the adaptive significance of worker production in the facultatively social small carpenter bee, Ceratina calcarata. Behav. Ecol. Sociobiol. 71, 135 (2017).

Woodard, S. H., Fischman, B. J., Venkat, A., Hudson, M. E. & Varala, K. Genes involved in convergent evolution of eusociality in bees. Proc. Natl Acad. Sci. 108, 7472–7477 (2011).

Sadd, B. M. et al. The genomes of two key bumblebee species with primitive eusocial organization. Genome Biol. 16, 76 (2015).

Schwarz, M. P., Richards, M. H. & Danforth, B. N. Changing paradigms in insect social evolution: insights from halictine and allodapine bees. Annu. Rev. Entomol. 52, 127–150 (2007).

Blomberg, S. P. & Garland, T. Tempo and mode in evolution: phylogenetic inertia, adaptation and comparative methods. J. Evol. Biol. 15, 899–910 (2002).

Hansen, T. F. & Orzack, S. H. Assessing current adaptation and phylogenetic inertia as explanations of trait evolution: the need for controlled comparisons. Evolution 59, 2063–2072 (2005).

Sakagami, S. F. & Maeta, Y. Multifemale nests and rudimentary castes in the normally solitary bee Ceratina japonica (Hymenoptera: Xylocopinae). J. Kans. Entomol. Soc. 57, 639–656 (1984).

Sakagami, S. F. & Maeta, Y. Multifemale nests and rudimentary castes of an “almost” solitary bee Ceratina flavipes, with additional observation on multifemale nests of Ceratina japonica (Hymenoptera, Apoidea). Entomological Soc. Jpn. 55, 391–409 (1987).

Rehan, S. M. et al. Conserved genes underlie phenotypic plasticity in an incipiently social bee. Genome Biol. Evol. 10, 2749–2758 (2018).

Durant, D. R., Berens, A. J., Toth, A. L. & Rehan, S. M. Transcriptional profiling of overwintering gene expression in the small carpenter bee, Ceratina calcarata. Apidologie 47, 572–582 (2016).

Rehan, S. M., Berens, A. J. & Toth, A. L. At the brink of eusociality: transcriptomic correlates of worker behaviour in a small carpenter bee. BMC Evolut. Biol. 14, 260 (2014).

Rehan, S. M., Glastad, K. M., Lawson, S. P. & Hunt, B. G. The genome and methylome of a subsocial small carpenter bee, Ceratina calcarata. Genome Biol. Evol. 8, 1401–1410 (2016).

Withee, J. R. & Rehan, S. M. Social aggression, experience, and brain gene expression in a subsocial bee. Integr. Comp. Biol. 57, 640–648 (2017).

Shell, W. A. & Rehan, S. M. The price of insurance: costs and benefits of worker production in a facultatively social bee. Behav. Ecol. 29, 204–211 (2018).

Shell, W. A. & Rehan, S. M. Social modularity: conserved genes and regulatory elements underlie caste-antecedent behavioural states in an incipiently social bee. Proc. R. Soc. B 286, 20191815 (2019).

Steffen, M. A. & Rehan, S. M. Genetic signatures of dominance hierarchies reveal conserved cis-regulatory and brain gene expression underlying aggression in a facultatively social bee. Genes Brain Behav. 19, e12597 (2020).

Dogantzis, K. A. et al. Insects with similar social complexity show convergent patterns of adaptive molecular evolution. Sci. Rep. 8, 10388 (2018).

Kent, C. F., Minaei, S., Harpur, B. A. & Zayed, A. Recombination is associated with the evolution of genome structure and worker behavior in honey bees. Proc. Natl Acad. Sci. USA 109, 18012–18017 (2012).

Harpur, B. A. et al. Population genomics of the honey bee reveals strong signatures of positive selection on worker traits. Proc. Natl Acad. Sci. USA 111, 2614–2619 (2014).

Chandrasekaran, S. et al. Behavior-specific changes in transcriptional modules lead to distinct and predictable neurogenomic states. Proc. Natl Acad. Sci. 108, 18020–18025 (2011).

Boetzer, M., Henkel, C. V., Jansen, H. J., Butler, D. & Pirovano, W. Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 27, 578–579 (2011).

Boetzer, M. & Pirvano, W. Toward almost closed genomes with GapFiller. Genome Biol. 13, R56 (2012).

Haas, B. J. et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 8, 1494 (2013).

Simão, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V. & Zdobnov, E. M. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31, 3210–3212 (2015).

Holt, C. & Yandell, M. MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects. BMC Bioinform. 12, 491 (2011).

De Bie, T., Cristianini, N., Demuth, J. P. & Hahn, M. W. CAFE: a computational tool for the study of gene family evolution. Bioinformatics 22, 1269–1271 (2006).

Sánchez-Garcia, A., Vieira, F. G. & Rozas, J. Molecular evolution of the major chemosensory gene families in insects. Heredity 103, 208–216 (2009).

Wittwer, B. et al. Solitary bees reduce investment in communication compared with their social relatives. Proc. Natl Acad. Sci. USA 114, 6569–6574 (2017).

Zhou, X. et al. Chemoreceptor evolution in Hymenoptera and its implications for the evolution of eusociality. Genome Biol. Evol. 7, 2407–2416 (2015).

Scott, J. G. & Wen, Z. Cytochromes P450 of insects: the tip of the iceberg. Pest Manag. Sci. 57, 958–967 (2001).

Hoffmann, K., Gowin, J., Hartfelder, K. & Korb, J. The scent of royalty: a P450 gene signals reproductive status in a social insect. Mol. Biol. Evol. 31, 2689–2696 (2014).

Cremer, S., Pull, C. D. & Fürst, M. A. Social immunity: emergence and evolution of colony-level disease protection. Annu. Rev. Entomol. 63, 105–123 (2019).

Yang, Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586–1591 (2007).

Li-Byarlay, H. & Cleare, X. Current trends in the oxidative stress and ageing of social hymenopterans. Adv. In Insect Phys. 59, 43–69 (2020).

Arendsee, Z. et al. phylostratr: A framework for phylostratigraphy. Bioinformatics 35, 3617–3627 (2019).

Johnson, B. R. & Tsutsui, N. D. Taxonomically restricted genes are associated with the evolution of sociality in the honey bee. BMC Genomics 12, 164 (2011).

Behl, S., Wu, T., Chernyshova, A. M. & Thompson, G. J. Caste-biased genes in a subterranean termite are taxonomically restricted: implications for novel gene recruitment during termite caste evolution. Insectes Sociaux 65, 593–599 (2018).

Cronin, A. L. & Schwarz, M. P. Latitudinal variation in the life cycle of allodapine bees (Hymenoptera Apidae). Can. J. Zool. 77, 857–864 (1999).

Rehan, S. M., Richards, M. H. & Schwarz, M. P. Social polymorphism in the Australian small carpenter bee. Ceratina (Neoceratina) australensis. Insect Soc. 57, 403–412 (2010).

Hurst, P. S. Social biology of Exoneurella tridentata, an allodapine bee with morphological castes and perennial colonies. Unpublished D. Phil. Thesis, Flinders University (2001).

Robinson, G. E., Fernald, R. D. & Clayton, D. F. Genes and social behavior. Science 322, 896–900 (2011).

Singh, A. S., Shah, A. & Brockmann, A. Honey bee foraging induces upregulation of early growth response protein 1, hormone receptor 38 and candidate downstream genes of the ecdysteroid signaling pathway. Insect Mol. Biol. 27, 90–98 (2018).

Shah, A., Jain, R. & Brockmann, A. Egr-1: a candidate transcription factor involved in molecular processes underlying time-memory. Front. Psychol. 9, 865 (2018).

Molodtsova, D., Harpur, B. A., Kent, C. F., Seevananthan, K. & Zayed, A. Pleiotropy constrains the evolution of protein but not regulatory sequences in a transcription regulatory network influencing complex social behaviors. Front. Genet. 5, 431 (2014).

Berens, A. J., Hunt, J. H. & Toth, A. L. Comparative transcriptomics of convergent evolution: different genes but conserved pathways underlie caste phenotypes across lienages of eusocial insects. Mol. Biol. Evol. 32, 690–703 (2014).

Anders, S. & Huber, W. Differential expression analysis for sequence count data. Genome Biol. 11, R106 (2010).

Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).

Alexa, A. & Rahnenfuhrer, J. topGO: enrichment analysis for gene ontology. R package version 2.28.0. CRAN (2016).

Sinha, S., Liang, Y. & Siggia, E. Stubb: a program for discovery and analysis of cis-regulatory modules. Nucleic Acids Res. 34, W555–W559 (2006).

Ament, S. A. et al. New meta-analysis tools reveal common transcriptional regulatory basis for multiple determinants of behavior. Proc. Natl Acad. Sci. USA 109, E1801–E1810 (2012).

Bossert, S. et al. Combining transcriptomes and ultraconserved elements to illuminate the phylogeny of Apidae. Mol. Phylogenet. Evol. 130, 121–131 (2019).


Colony Size Evolution and the Origin of Eusociality

Our results, based on analyses that evaluated the phylogenetic uncertainty, and the reconstruction of ancestral states, show that the colony size of corbiculate bees coevolves with the level of sociality ( Fig. 2 , ​ ,3 3 Table 2 ). Colony size is a complex trait, determined by various factors that favor or restrict the number of individuals [1]. Those which restrict colony size are associated with traits related to life history [21], periodicity of trophic resources and space for nesting [22], among others. These multiple factors have differential importance throughout the tribes of Apinae. For example, with respect to the physical space for nesting [22]: the species in the Meliponini tribe prefer to use hollow trees for nesting, and there are also hypogeous species [23]. There is a strong spatially limiting factor involved in the development of highly large colonies, such as those of the Apini. Other factors could be influencing colony size in the Bombini tribe, especially factors correlated with latitude, due to the annual cycle of the colonies of this tribe [24], [25]. These ecological factors that determine the colony size could be responsible for the qualitative change from the most recent common ancestor (MRCA) of Apini + Euglossini ( Fig. 2 , node E: categorical 0 to 10 continuous 1.9 individuals) to the MRCA of Apini ( Fig. 2 , node A: categorical � continuous 11592 individuals).

The lack of intermediate form between these nodes does not have a straightforward interpretation. Some insight can be obtained from allodapine bees (Apidae: Allodapini), in which the colony size and the level of sociality is a function of environmental and ecological variables in the facultative eusocial Exoneurella tridentata (i.e. a xeric habitat and durable nesting substrate [26]). This bee is an exception within the tribe, given that it shows both a discrete morphological gap between queen and worker castes, and evolution of colony size (� females) with accelerated tempo [26], [27]. The colony size and eusociality evolution of E. tridentata thus represent a discontinuity in the evolutionary change of the Allopadini tribe, which could be associated with overcoming a strong selective barrier (sensu [26]). A barrier that could be important at the MRCA of Apini + Euglossini ( Fig. 2 node E), can be inferred from a general exploration of the main ecological traits of Euglossini vs Apini. Euglossini is a tribe of highly specialized bees on a few plant families that inhabits almost exclusively the Neotropics, whereas Apini is a tribe with a wide range of both food resources and distribution [18], [28]. For example, strong resource dependence has been detected in Euglossa nigropilosa, which preclude many communal nesting females [29]. This could imply that few individuals in a communal society ( Fig. 2 node E) can either take advantage of generalist traits and increase colony size, or hold the character state as consequence of specialization ( Fig. 2 nodes A, B). In the same way, the evolution from the communal MRCA of Apini + Euglossini ( Fig. 3 , node E) to the eusocial with morphological castes MRCA of Apini ( Fig. 3 , node A) can be addressed by scarce evidence from the halictine sweat bee Halictus sexcinctus (Hymenoptera: Halictidae [30]). This species shows a communal/eusocial polymorphism in the same population, where the eusocial colonies are composed of distinct morphological castes, which also differ from the communal foundresses [30]. Since the social polymorphism of H. sexcinctus is an extraordinary case within Halictidae, Richards et al. [30], argue that it may represent an unstable intermediate step in the evolution of social behavior. The consequences of this labile character state are either to promote some individuals to dominate reproduction or the founding of solitary colonies [30]. However, these species with facultative eusociality (E. tridentata and H. sexcinctus) show small incremental changes in colony size between the communal and eusocial states. The differential of colony size and level of sociality character states found on the transition from Node E to Node A ( Fig. 2 and ​ and3) 3 ) seem to be quite different. Then, explanations are needed beyond actual ecological forces for this.

Boomsma [31], [32] proposed that lifetime monogamous species are more likely to evolve obligate eusociality (i.e. eusocial with morphological castes). This hypothesis argues that in lifetime monogamous species, relatedness is maximized throughout the lives of helper cohorts, promoting the evolution of sterile caste [32]. The previous examples of allodapine and halictid bees only show an advanced form of cooperative breeding [32]. Although this proposal has been supported in a phylogenetic context, including the estimated character state at MRCA of corbiculate bees [16], further questions arise. For instance, once lifetime monogamy is established, how do sterile castes then evolve? In this context, the explanation for the transition between the MRCA of Apini + Euglossini to the MRCA of Apini, could be addressed from the reproductive abilities of a worker 𠇋y its own choice” [5]. The direct reproductive benefits tend to decrease, as well as the indirect benefits increase, while the colony grows in size. This is because the worker loses opportunities to replace the queen in a colony where more and more workers are trying to take over the colony [5], and, concurrently, this crowded colony represents a full-sibling system. Then, the benefits may outweigh the costs simply by increasing the number of individuals in a colony. Bourke [1] used an extended argument that incorporates the mutual inhibition between workers of their reproduction potential (i.e. worker policing, [2]). This behavior leads to the selection of highly specialized workers accompanied by morphological skew between castes, which at the same time incurs positive feedback, permitting the existence of larger colonies. If this mechanism operates, then it is not necessary that the ancestor of eusocial forms with morphological castes be eusocial with behavioral castes, only that it have a monogamous reproductive system. Based on our results, we suggest that it is possible for eusociality with morphological castes to evolve either from a gradual increase in colony size and complexity ( Fig. 2 from node F to node D), or from a threshold of colony size ( Fig. 2 from node E to node A). Once it has reached this character state, the species can’t revert, consistent with previous studies [32] ( Fig. 2 Node B, C).

Finally, our study, based on a Bayesian probabilistic framework, provides strong support for Bourke’s proposal [1] since we have observed that the one of the main determinants in the evolution of morphological castes in complex societies of corbiculate bees is colony size. The study of this trait improves our knowledge regarding the evolutionary transition from simple to complex societies, and highlights the importance of explicit probabilistic models to test the evolution of eusociality and other important characters in social species.


Phylogenetic Relationships of Corbiculate Bees

The phylogenetic reconstruction that best fit to the rates and patterns of molecular evolution of the data was that obtained with 2GTR+Γ matrices. The consensus tree topology showed corbiculate bees to be a completely sustained monophyletic group (Fig. 1, Node G), where each tribe corresponded to a highly supported natural group. The relationship between tribes was observed to have a higher posterior probability (Fig. 1, Node E and F). Our phylogenetic hypothesis has no differenced from that reported by Cardinal et al. [20], so is a good historical support for further comparative analysis.

The tree was obtained by means of a phylogenetic mixture model based on Bayesian approach. The numbers next to nodes indicate the posterior probability of occurrence of the clade. The letters above the nodes correspond to the hypothetical ancestors, whose most probable character state is shown in Figures 2 and 3.

Colony Size and Social Structure Evolution

The predominant evolutionary transition rates among the different colony size states were, q12, q21 (Table 1) that is, the transition from few to hundreds of individuals in both directions. In addition, the predominant transition rates in the evolution of sociality were q21, q12, (Table 1), that is, the transition from solitary to communal in both directions. The ancestral character state estimation for the phylogeny nodes indicated that the most probable common ancestor of the corbiculate bee tribes was a colony of few individuals (Fig. 2 Node G probability (p) = 0.51 1.7 individuals) with a communal sociality level (Fig. 3 Node G p = 0.44). The ancestor of the Meliponini and Bombini has a higher probability of having tens/hundreds of individuals (Fig. 2 Node F p = 0.51 18.9 individuals) and eusocial with behavioral castes (Fig. 3 Node F p = 0.68). On the other hand, the ancestor of Euglossini and Apini has more probability of having colonies with few individuals (Fig. 2, Node E p = 0.50 1.9 individuals) with a communal social structure (Fig. 3 Node E, p = 0.50).The development of morphological castes occurred independently in two lineages: In the Meliponini ancestor (Fig. 3 Node D, p = 0.99) and in the Apini ancestor (Fig. 3 Node A, p = 0.98). The ancestors of both tribes had large colonies (Fig. 2 Node A p = 0.54 11592 individuals and Node D p = 0.83 2077 individuals).

The reconstruction was based on both topology and branch lengths of the Bayesian phylogenetic trees. In parenthesis is shown the mean value and standard error for the continuous character reconstruction.

The reconstruction was based on both the topology and branch lengths of the Bayesian phylogenetic trees.

Finally, the results of the phylogenetic logistic regression show that the effect of colony size on social structure is significantly different from zero if the evolutionary relationships of corbiculate bees are part of the model (Table 2). Larger values of colony size are strongly related to more complex social structure (i.e. eusocial with morphological castes Table 2, b1 = 7.7475 p<0.001). Concordantly, smaller colony sizes are strongly related with the absence of complex societies (i.e. eusocial with behavioral/morphological castes Table 2, b1 = −2.2793 p<0.001).

Broader Implications

In the ants and other social insects, we are thus privileged to see not only how complex societies have evolved independently of those of humans and in a different sensory modality (mostly chemosensory versus audiovisual) but also, with increasing clarity, the relations between levels of biological organization and the forces of natural selection that formed and shaped them. We have also begun to glimpse, albeit still dimly and in fragments, connections between major features of the sociobiology, ecology, and biogeography of these insects.

If the conclusions drawn here about eusociality in insects and other arthropods are correct, they could have implications for advanced social behavior outside the arthropods. Rarity and the preeminence of group selection in unusual environments that favor cooperation are shared by the bathyergid rodents, the only highly eusocial phylad known in the vertebrates. Rarity of occurrence and unusual preadaptations characterized the early species of Homo and were followed in a similar manner during the advancement of the ants and termites by the spectacular ecological success and preemptive exclusion of competing forms by Homo sapiens.

Watch the video: How a Bee Becomes Queen (May 2022).