Information use in colonial living

Despite the fact that many animals live in groups, there is still no clear consensus about the ecological or evolutionary mechanisms underlying colonial living. Recently, research has suggested that colonies may be important as sources of social information. The ready availability of information from conspecifics allows animals to make better decisions about avoiding predators, reducing brood parasitism, migratory phenology, mate choice, habitat choice and foraging. These choices can play a large part in the development and maintenance of colonies. Here we review the types of information provided by colonial animals and examine the different ways in which decision‐making in colonies can be enhanced by social information. We discuss what roles information might take in the evolution, formation and maintenance of colonies. In the process, we illustrate that information use permeates all aspects of colonial living.     

Coexistence and displacement in consumer-resource systems with local and shared resources

Competition for local and shared resources is widespread. For example, colonial waterbirds consume local prey in the immediate vicinity of their colony, as well as shared prey across multiple colonies. However, there is little understanding of conditions facilitating coexistence vs. displacement in such systems. Extending traditional models based on type I and type II functional responses, we simulate consumer-resource systems in which resources are “substitutable,” “essential,” or “complementary.” It is shown that when resources are complementary or essential, a small increase in carrying capacity or decrease in handling time of a local resource may displace a spatially separate consumer species, even when the effect on shared resources is small. This work underscores the importance of determining both the nature of resource competition (substitutable, essential, or complementary) and appropriate scale-dependencies when studying metacommunities. We discuss model applicability to complex systems, e.g., urban wildlife that consume natural and anthropogenic resources which may displace rural competitors by depleting shared prey.     

Breeding colonies as information centers: a reappraisal of information-based hypotheses using the producer--scrounger game

One of the most cited hypotheses for the evolutionary advantagesof colonial breeding proposes that colonies serve as a placeof information exchange about the location of food—theinformation center hypothesis. Despite its popularity, thehypothesis generated considerable controversy over its predictionsand role in the evolution of colonial breeding. As a consequence,the hypothesis still lingers on, despite numerous apparent falsifications from both observational and experimental approaches.The controversy has three roots: the unclear causal directionbetween coloniality and information center, the unrecognizeddistinction between colonial breeding and colonial roosting,and the use of an implicit group selectionist argument. Herewe try to clarify this controversy by applying an entirely individual selection-based approach, the producer-scrounger game, to theinformation center hypothesis. Furthermore, we show how otherinformation-based alternatives of the original informationcenter hypothesis (e.g., local enhancement and recruitmentcenter hypotheses) can be included in a common framework. Ourmodel predicts that individuals relying on information transfer at the colony should be rather common in nature. This predictionis essentially unaltered by the inclusion of either local enhancementor recruitment center. On the other hand, the frequency ofleading unknowledgeable individuals (the most accepted signof information center) is expected to be very low. The modelindicates that tests of information-based hypotheses shouldfocus on the expected relative frequency of food-searching flights rather than the frequency of leading.     

Smelling like resin: terpenoids account for species-specific cuticular profiles in Southeast-Asian stingless bees

Insects may be unique in having a cuticle with a species-specific chemical profile. In social insects, colony survival depends not only on species-specific but also on colony-specific cuticular compounds with hydrocarbons playing an important role in the communication systems of ants, termites, wasps and bees. We investigated inter- and intraspecific differences in the composition of compounds found on the body surface of seven paleotropical stingless bee species (Apidae: Meliponini) at two different sites in Borneo (Sabah, Malaysia). Besides hydrocarbons, the body surface of all seven stingless bee species comprised terpenoid compounds, a substance class that has not been reported for chemical profiles of any social insect so far. Moreover, the chemical profile of some species differed fundamentally in the composition of terpenoids with one group (e.g. sesquiterpenes) being present in one species, but missing in another. Chemical profiles of different colonies from the same species showed the same hydrocarbon- and terpenoid compounds over different regions, as tested for Tetragonilla collina and Tetragonula melanocephala. However, chemical profiles differed quantitatively between the different colonies especially in T. melanocephala. It is likely that the terpenoids are derived from plant resins because stingless bees are known to collect and use large amounts of resins for nest construction and defence, suggesting an environmental origin of the terpenoids in the chemical profile of paleotropical stingless bees.     

Do multi-branched colonial organisms exceed normal growth after partial mortality?

One of the advantages of modular colonial growth is the capability to recover after partial mortality. Tolerance to partial mortality is a known property of some resistant species of plants that respond to mortality with vigorous regrowth or overcompensation. It is not clear whether modular marine invertebrates such as octocorals overcompensate. This study provides evidence that following injury to colonies (by breaking apical dominance), new growth exceeds normal rates of branching, as observed in some plants, in a degree correlated to the original multi-branched network setting (e.g. the number of original branches connected to main stem), in colonies of the Caribbean gorgonian octocoral Pseudopterogorgia bipinnata. This can be explained by the network of communicating vessels and canals inside octocoral colonies, which provide the structure for effective allocation of resources to regenerating parts.     

Genome-wide signatures of mammalian skin covering evolution

Animal body coverings provide protection and allow for adaptation to environmental pressures such as heat, ultraviolet radiation,water loss, and mechanical forces. Here, using a comparative genomics analysis of 39 mammal species spanning three skin covering types(hairless, scaly and spiny), we found some genes(e.g., UVRAG, POLH, and XPC) involved in skin inflammation,skin innate immunity, and ultraviolet radiation damage repair were under selection in hairless ocean mammals(e.g., whales and manatees). These signatures might be associated with a high risk of skin diseases from pathogens and ultraviolet radiation.Moreover, the genomes from three spiny mammal species shared convergent genomic regions(EPHB2, EPHA4, and NIN) and unique positively selected genes(FZD6, INVS, and CDC42) involved in skin cell polarity, which might be related to the development of spines. In scaly mammals, the shared convergent genomic regions(e.g., FREM2) were associated with the integrity of the skin epithelium and epidermal adhesion. This study identifies potential convergent genomic features among distantly related mammals with the same skin covering type.     

Essential conditions for evolution of communication within a species

A major obstacle in analyzing the evolution of information exchange and processing is our insufficient understanding of the underlying signaling and decision-making biological mechanisms. For instance, it is unclear why are humans unique in developing such extensive communication abilities. To treat this problem, a method based on the mutual information approach is developed that evaluates the information content of communication between interacting individuals through correlations of their behavior patterns (rather than calculating the information load of exchanged discrete signals, e.g. Shannon entropy). It predicts that correlated interactions of the indirect reciprocity type together with affective behavior and selection rules changing with time are necessary conditions for the emergence of significant information exchange. Population size variations accelerate this development. These results are supported by evidence of demographic bottlenecks, distinguishing human from other species’ (e.g. apes) evolution line. They indicate as well new pathways for evolution of information based phenomena, such as intelligence and complexity.     

Effect of flow regime on the morphology of a colonial cnidarian

Abstract. Phenotypic plasticity is the ability of some organisms to exhibit different phenotypes in response to environmental conditions. Many sessile marine invertebrates are morphologically plastic. In colonial cnidarians, compact morphologies are often associated with high-velocity flow regimes, whereas elongated morphologies are associated with calmer water. This ability to alter morphology in response to flow regime likely represents an adaptive strategy: these morphologies may permit efficient suspension feeding and gas exchange while reducing the risk of dislodgment in a particular flow regime. Which flow-related factors (e.g., CO₂ accumulation, drag forces, prey delivery) actually signal a colony to alter its morphology are unclear. In this study, we test the hypothesis that differences in flow regime or some correlate of flow regime (in the absence of differences in prey delivery) signal a colonial cnidarian to change its morphology. To separate prey delivery from water flow, hydroid ( Bougainvillia muscus ) colonies were fed equivalent amounts in still water, regardless of the flow regime treatment to which they were exposed the rest of the time. Our results show that, regardless of prey delivery, colonies grew in ways characteristic of calm water (with a higher percentage of tall pedicels and secondary hydranths, and fewer basal stolon branches) and of high flow (with more hydranths, free stolons, and a denser basal stolon network) environments. This work suggests that, for this hydroid, prey flux is not a proximate cue mediating morphological plasticity in response to flow regime.     

cot-1, a gene required for hyphal elongation in Neurospora crassa, encodes a protein kinase.

Neurospora crassa is a filamentous fungus that grows on semisolid media by forming spreading colonies. Mutations at several loci prevent this spreading growth. cot-1 is a temperature sensitive mutant of N.crassa that exhibits restricted colonial growth. At temperatures above 32 degrees C colonies are compact while at lower temperatures growth is indistinguishable from that of the wild type. Restricted colonial growth is due to a defect in hyphal tip elongation and a concomitant increase in hyphal branching. We have isolated a genomic cosmid clone containing the wild type allele of cot-1 by complementation. Sequence analyses suggested that cot-1 encodes a member of the cAMP-dependent protein kinase family. Strains in which we disrupted cot-1 are viable but display restricted colonial growth. Duplication, by ectopic integration of a promoter-containing fragment which includes the first one-third (209 codons) of the structural gene, unexpectedly resulted in restricted colonial growth. Our results suggest that an active COT1 kinase is required for one or more events essential for hyphal elongation.     

Outlier analyses to test for local adaptation to breeding grounds in a migratory arctic seabird

Investigating the extent (or the existence) of local adaptation is crucial to understanding how populations adapt. When experiments or fitness measurements are difficult or impossible to perform in natural populations, genomic techniques allow us to investigate local adaptation through the comparison of allele frequencies and outlier loci along environmental clines. The thick‐billed murre (Uria lomvia) is a highly philopatric colonial arctic seabird that occupies a significant environmental gradient, shows marked phenotypic differences among colonies, and has large effective population sizes. To test whether thick‐billed murres from five colonies along the eastern Canadian Arctic coast show genomic signatures of local adaptation to their breeding grounds, we analyzed geographic variation in genome‐wide markers mapped to a newly assembled thick‐billed murre reference genome. We used outlier analyses to detect loci putatively under selection, and clustering analyses to investigate patterns of differentiation based on 2220 genomewide single nucleotide polymorphisms (SNPs) and 137 outlier SNPs. We found no evidence of population structure among colonies using all loci but found population structure based on outliers only, where birds from the two northernmost colonies (Minarets and Prince Leopold) grouped with birds from the southernmost colony (Gannet), and birds from Coats and Akpatok were distinct from all other colonies. Although results from our analyses did not support local adaptation along the latitudinal cline of breeding colonies, outlier loci grouped birds from different colonies according to their non‐breeding distributions, suggesting that outliers may be informative about adaptation and/or demographic connectivity associated with their migration patterns or nonbreeding grounds.     

Evolution and dynamics of branching colonial form in marine modular cnidarians: gorgonian octocorals

Multi-branched arborescent networks are common patterns for many sessile marine modular organisms but no clear understanding of their development is yet available. This paper reviews new findings in the theoretical and comparative biology of branching modular organisms (e.g. Octocorallia Cnidaria) and new hypotheses on the evolution of form are discussed. A particular characteristic of branching Caribbean gorgonian octocorals is a morphologic integration at two levels of colonial organization based on whether the traits are at the module or colony level. This revealed an emergent level of integration and modularity produced by the branching process itself and not entirely by the module replication. In essence, not just a few changes at the module level could generate changes in colony architecture, suggesting uncoupled developmental patterning for the polyp and branch level traits. Therefore, the evolution of colony form in octocorals seems to be related to the changes affecting the process of branching. Branching in these organisms is sub-apical, coming from mother branches, and the highly self-organized form is the product of a dynamic process maintaining a constant ratio between mother and daughter branches. Colony growth preserves shape but is a logistic growth-like event due to branch interference and/or allometry. The qualitative branching patterns in octocorals (e.g. sea feathers, fans, sausages, and candelabra) occurred multiple times when compared with recent molecular phylogenies, suggesting independence of common ancestry to achieve these forms. A number of species with different colony forms, particularly alternate species (e.g. sea candelabrum), shared the same value for an important branching parameter (the ratio of mother to total branches). According to the way gorgonians branch and achieve form, it is hypothesized that the diversity of alternate species sharing the same narrow variance in that critical parameter for growth might be the product of canalization (or a developmental constraint), where uniform change in growth rates and maximum colony size might explain colony differences among species. If the parameter preserving shape in the colonies is fixed but colonies differ in their growth rates and maximum sizes, heterochrony could be responsible for the evolution among some gorgonian corals with alternate branching.     

Task-Related Variation of Cuticular Hydrocarbon Profiles Affect Nestmate Recognition in the Giant ant Dinoponera quadriceps

Recognition seems to be one of the more remarkable characteristics of social groups. In social insects, cuticular hydrocarbons are important for colonial recognition by providing a chemical signature for colony members. The acceptance threshold model predicts that colony members will accept conspecifics when the levels of nest mate cues dissimilarities are below the acceptance threshold. We tested the hypothesis that the encounter of a guard ant worker with a nurse may cause a delay in the process of recognition, because nurses from distinct colonies may share greater amount of chemical compounds. Dinoponera quadriceps guard workers decreased their effectiveness to recognize nurses rather than did to foragers. Alien foragers received significantly more bites and other stronger acts than non-nestmate nurses when they were experimentally introduced. In addition, guards took significantly more time to react against non-nestmate nurses than against alien foragers. Analysis of the cuticular hydrocarbon profiles corroborated our behavioural analysis that nurses from distinct colonies overlap greater amount of cuticular hydrocarbons.     

Effects of juvenile hormone analogs on new reproductives and colony growth of Pharaoh ant (Hymenoptera: Formicidae)

Two juvenile hormone analogs (JHAs), pyriproxyfen and S-methoprene, were impregnated into dried tuna fish and fed to colonies of Monomorium pharaonis (L.) at very low concentrations (1.0, 2.0, 3.0, 4.0, and 5.0 microg/ml). Its effects on the production of sexuals and colonial growth were observed. Colonies treated with pyriproxyfen yielded sexuals with physical abnormalities. Both female and male sexuals developed bulbous wings, decreased melanization, and died shortly after emergence. Sexuals emerged from colonies treated with S-methoprene did not possess anomalous characteristics. Both pyriproxyfen and S-methoprene did not have significant effects on colonial growth because of the low concentrations of the baits. A commercial bait containing 0.3% S-methoprene (Bioprene-BM) also was evaluated for its efficacy on Pharaoh's ant colonies. Results showed that Pharaoh's ant colonies succumbed to the lethal effects of S-methoprene. Colony members were reduced significantly. Production of queens also decreased significantly in treated colonies and treated queens were unable to lay eggs. JHAs are slow acting and eliminate ant colonies at a relatively slow rate. At low concentrations, pyriproxyfen recorded baffling results, i.e., bulbous wings and demelanized exoskeleton, and it is vital that further studies are initiated to solidify these findings.     

Iterative evolution of increased behavioral variation characterizes the transition to sociality in spiders and proves advantageous

Abstract The evolution of group living is regarded as a major evolutionary transition and is commonly met with correlated shifts in ancillary characters. We tested for associations between social tendency and a myriad of abiotic variables (e.g., temperature and precipitation) and behavioral traits (e.g., boldness, activity level, and aggression) in a clade of spiders that exhibit highly variable social structures (genus Anelosimus). We found that, relative to their subsocial relatives, social species tended to exhibit reduced aggressiveness toward prey, increased fearfulness toward predators, and reduced activity levels, and they tended to occur in warm, wet habitats with low average wind velocities. Within-species variation in aggressiveness and boldness was also positively associated with sociality. We then assessed the functional consequences of within-species trait variation on reconstituted colonies of four test species (Anelosimus eximius, Anelosimus rupununi, Anelosimus guacamayos, and Anelosimus oritoyacu). We used colonies consisting of known ratios of docile versus aggressive individuals and group foraging success as a measure of colony performance. In all four test species, we found that groups composed of a mixture of docile and aggressive individuals outperformed monotypic groups. Mixed groups were more effective at subduing medium and large prey, and mixed groups collectively gained more mass during shared feeding events. Our results suggest that the iterative evolution of depressed aggressiveness and increased within-species behavioral variation in social spiders is advantageous and could be an adaptation to group living that is analogous to the formation of morphological castes within the social insects.     

Colonial allorecognition,hemolytic rejection,and viviparity in botryllid ascidians

Allorecognition is a fundamental system that animals use to maintain individuality. Although embryos are usually semiallogeneic with their mother, viviparous animals are required to allow these embryos to develop inside the maternal body, but must also eliminate an "invasion" by nonself. In colonial ascidians of the family Botryllidae, when two colonies are brought into contact at their growing edges, a hemolytic rejection reaction occurs between allogeneic colonies. Morula cells, a type of hemocyte, are the major effector cells in the hemolytic rejection. Morula cells infiltrate and aggregate where the two colonies make contact, and then discharge their vacuolar contents, which contain phenoloxidase and quinones. In viviparous botryllids, colonial contact at artificially cut surfaces always results in colonial fusion and establishment of a common vascular network even between allogeneic colonies in which the growing-edge contact results in rejection. This colonial fusion between incompatible colonies (surgical fusion) suggests that the allorecognition sites are not distributed in the vascular system in which the embryos are brooded. It is supposed that a common ancestor of the viviparous species lost the capacity for allorecognition in their vascular system to protect its embryos from alloreactivity, when it changed from ovoviviparous to viviparous in the course of evolution. The limited distribution of allorecognition sites would be a solution to the embryo-parent histoincompatibility in viviparity.     

Cloning and characterization of BS-cadherin, a novel cadherin from the colonial urochordate Botryllus schlosseri

The genomic DNA for a novel member of the cadherin family (BS-cadherin) was cloned and characterized from the colonial marine invertebrate, Botryllus schlosseri. Using a differential display of mRNA by means of PCR, a small cDNA fragment of 380 nucleotides was found to be specifically expressed in a colony undergoing allogeneic rejection processes, as compared with naïve parts of the same genotype. This cDNA fragment was used as a probe to screen a genomic library of Botryllus schlosseri. A genomic fragment containing an ORF of 2718 nucleotides, with no introns, was isolated. The encoded protein exhibits a typical structure of cadherins; an extracellular domain with conserved repeated sequences (cadherin signatures), a single transmembrane domain and a conserved cytoplasmic tail region. The BS-cadherin amino-acid sequence shows 32–35% identity to mature classical cadherins type I, e.g., N-, P- and E-cadherin as well as mature classical cadherins type II, e.g., human cadherin-6, -8 and OB-cadherin. This cadherin represents a new cadherin gene family, evolutionarily distant to all other known classical cadherins.     

Variation of colony types in the antFormica cinerea

Summary Formica cinerea is a rare ant species in northern Europe where it occurs in few isolated populations. Estimates of genetic relatedness among worker nestmates revealed very different colonial structures. Relatedness was g = 0.81 in one population, and g = –0.03 and = 0.01 in two others. These results indicate that some populations of the species have mainly monogynous colonies (perhaps with monandrous queens), whereas others consist of polygynous and possibly polydomous colonies. Genetic differentiation of closely located populations suggests restricted dispersal.     

Hydrocarbon circulation and colonial signature in Pachycondyla villosa

In ants, both cuticular and postpharyngeal gland (PPG) hydrocarbons (HCs) have been involved in nestmate recognition. However, no detailed comparison is available. A comparative study including also high density lipophorin (HDLp), an internal HC carrier, was therefore undertaken on Pachycondyla villosa. Purified HDLp is an 820 kDa lipoprotein with a density of 1.114 g/ml and two 245 and 80 kDa apo-proteins. Its hydrocarbon profile is very similar with the cuticular one, in agreement with its hydrocarbon carrier function. Conversely, n-alkanes and externally branched monomethylalkanes are markedly decreased in the PPG. According to their physical properties, this suggests that they are involved in waterproofing on the cuticle. The PPG actually contains only internally branched mono-, dimethylalkanes or monomethylalkenes; their greater fluidity is more adequate for chemical communication. The percentages of some of them are statistically not different between the cuticle and PPG. Their mixtures vary with colonies and they may thus be involved in colonial signature. A scheme for hydrocarbon circulation is discussed, involving lipophorin, cuticle, PPG and self-grooming in one individual, a pathway complementary or alternative to the selective delivery by lipophorin in some other insects. HCs are then distributed between nestmates' cuticles through allo-grooming and physical contacts.     

Cooperative bird differentiates between the calls of different individuals, even when vocalizations were from completely unfamiliar individuals

Hypotheses proposed to explain the evolution of cooperative behaviour typically require differentiation between either groups of conspecifics (e.g. kin/non-kin) or, more typically, individuals (e.g. reciprocal altruism). Despite this, the mechanisms that facilitate individual or class recognition have rarely been explored in cooperative species. This study examines the individual differentiation abilities of noisy miners (Manorina melanocephala), a species with one of the most complex avian societies known. Miners permanently occupy colonies numbering into hundreds of individuals. Within these colonies, cooperative coalitions form on a fission-fusion basis across numerous contexts, from social foraging through to mobbing predators. Birds often use individually distinctive 'chur' calls to recruit others to a caller's location, facilitating coalition formation. I used the habituation-discrimination paradigm to test the ability of miners to differentiate between the chur calls of two individuals that were both either: (i) familiar, or (ii) unfamiliar to the focal subject. This technique had not, to my knowledge, been used to assess vocalization differentiation in cooperative birds previously, but here demonstrated that miners could correctly use the spectral features of signals to differentiate between the vocalizations of different individuals, regardless of their familiarity. By attending to individual differences in recruitment calls, miners have a communication system that is capable of accommodating even the most complex cooperative hypotheses based upon acoustic information.     

Social and genetic characteristics of geographically isolated populations in the ant Formica cinerea

The ant Formica cinerea in northern Europe has geographically isolated populations that were examined using five microsatellite loci. The populations differ widely regarding the social organization of colonies. Based on genetic relatedness (r) among worker nest mates, the populations were classified as M type with monogynous (single queen) colonies (r > 0.59), as P type with polygynous colonial networks (r < 0.1), or as intermediate with weakly polygynous colonies (0.16 < r < 0.47). The social types showed weak geographical clustering, but the overall distribution indicated that the shift between the social types has occurred several times. The geographically isolated populations had slightly reduced levels of genetic diversity compared to populations from areas where the species is abundant and continuously distributed. Many of the isolated populations consisted of monogynous or weakly polygynous colonies, making their effective population sizes small, and some of them also showed weak bottleneck effects. The overall level of microsatellite diversity within populations was relatively high and differentiation among populations low, indicating recent connections. Isolation of populations may thus be a new phenomenon resulting from reduction of suitable habitats. At the local level, we obtained limited support from a group of nearby subpopulations in southern Finland to the hypothesis that the P type is connected to restricted dispersal. Other P type populations did not, however, show similar elevated levels of differentiation.