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No major difference in growth and productivity between monogynous and polygynous colonies in the ant Myrmecina graminicola
Abstract
In ants, which are all eusocial, social polymorphism exists in the form of a variable number of queens. The occurrence of colonies with a single queen (monogynous) or multiple queens (polygynous) within a species is found in about 15% of ant species, offering various model systems to assess the life-history differences between the two social forms. Polygynous colonies are assumed to be better competitors due to larger colony size and higher colony growth, whereas monogynous colonies are supposed to rely on a colonizer strategy as they are founded solitarily by larger winged queens that disperse by flight. The ant Myrmecina graminicola harbors a social polymorphism associated with a wing polymorphism in queens, both being determined by a different supergene with monogynous queens being mostly winged and polygynous queens being always apterous. By comparing colonies sampled in the same population, we showed that polygynous colonies with apterous queens and monogynous colonies with winged queens did not differ in the number of workers and larvae at the time of collection. Accordingly, once reared in the laboratory, these colonies produced a similar number of pupae and adults (workers or sexual individuals), probably from the larvae already present at the time of collection. However, polygynous colonies produced more eggs and new larvae in the laboratory than their monogynous counterparts. We discuss why this larger brood production of polygynous colonies was not reflected by a larger colony size in the field, and what the consequences of similar colony growth and productivity between the social forms would mean for the maintenance of genetic polymorphisms.
Antagonistic selection has long been considered a major driver of the formation and expansion of sex chromosomes. For example, sexually antagonistic variation on an autosome can select for suppressed recombination between that autosome and the sex chromosome, leading to a neo-sex chromosome. Autosomal supergenes, chromosomal regions containing tightly linked variants affecting the same complex trait, share similarities with sex chromosomes, raising the possibility that sex chromosome evolution models can explain the evolution of genome structure and recombination in other contexts. We tested this premise in a Formica ant species, wherein we identified four supergene haplotypes on chromosome 3 underlying colony social organization and sex ratio. We discovered a novel rearranged supergene variant (9r) on chromosome 9 underlying queen miniaturization. The 9r is in strong linkage disequilibrium with one chromosome 3 haplotype (P 2 ) found in multi-queen (polygyne) colonies. We suggest that queen miniaturization is strongly disfavored in the single-queen (monogyne) background and is thus socially antagonistic. As such, divergent selection experienced by ants living in alternative social ‘‘environments’’ (monogyne and polygyne) may have contributed to the emergence of a genetic polymorphism on chromosome 9 and associated queen-size dimorphism. Consequently, an ancestral polygyne-associated haplotype may have expanded to include the polymorphism on chromosome 9, resulting in a larger region of suppressed recombination spanning two chromosomes. This process is analogous to the formation of neo-sex chromosomes and consistent with models of expanding regions of suppressed recombination. We propose that miniaturized queens, 16%–20% smaller than queens without 9r, could be incipient intraspecific social parasites.
Dispersal strategies are highly variable. Any strategy is associated to costs and benefits, and understanding which factors favour or disfavour a strategy is a key issue in ecology and evolution. Ants exhibit different dispersal and colony foundation strategies. Some species have winged queens that disperse solitarily and far by flight, and that found new colonies alone. Others have apterous queens that disperse with workers over short walking distances, and found new colonies as a group (colony fission). The putative benefits conferred by workers have been little studied and quantified, because comparing the costs and benefits of solitary vs. group dispersal and foundation is difficult when comparing different species. We did this using the ant Myrmecina graminicola, one of the few species that use both strategies. Young queens were mated and allowed to found new colonies in the laboratory, with either zero, two or four workers. We monitored the survival and growth of foundations over one year. The presence of workers increased both survival and growth, with more workers yielding higher growth. These results show the benefit of dispersing and founding in a group. The presence of few workers (as little as two workers) was sufficient to provide benefits, suggesting group foundation does not require a dramatic decrease in the number of propagules produced in M. graminicola. Our results support the hypothesis that the two strategies coexist along a competition-colonization trade-off, where solitary foundation offers a colonization advantage while group foundation has a competitive advantage.
Ant colonies ancestrally contained one queen and her non-reproductive workers. This is also the case for many but not all colonies of the Mediterranean big-headed ant Pheidole pallidula. Indeed, this species also has a derived form of social organization with multiple reproductive queens in the colony. The co-existence of two social forms also independently evolved in three other lineages of ants. In each of those lineages, variants of a supergene region of suppressed recombination determine social form. This is likely because supergene regions can link advantageous combinations of alleles from multiple loci. We thus hypothesized that a supergene region also determines colony queen number in the big-headed ant. To test this, we performed extensive population genetic analyses and genomic comparisons. We find no evidence of a supergene-like region with differentiation between single- and multiple-queen colonies. Our results show that a complex social polymorphism can evolve and be maintained without supergenes.
Species commonly exhibit alternative morphs, with individual fate being determined during development by either genetic factors, environmental cues or a combination thereof. Ants offer an interesting case study because many species are polymorphic in their social structure. Some colonies contain one queen while others contain many queens. This variation in queen number is generally associated with a suite of phenotypic and life-history traits, including mode of colony founding, queen lifespan, queen–worker dimorphism and colony size. The basis of this social polymorphism has been studied in five ant lineages, and remarkably social morph seems to be determined by a supergene in all cases. These ‘social supergenes’ tend to be large, having formed through serial inversions, and to comprise hundreds of linked genes. They have persisted over long evolutionary timescales, in multiple lineages following speciation events, and have spread between closely related species via introgression. Their evolutionary dynamics are unusually complex, combining recessive lethality, spatially variable selection, selfish genetic elements and non-random mating. Here, we synthesize the five cases of supergene-based social polymorphism in ants, highlighting interesting commonalities, idiosyncrasies and implications for the evolution of polymorphisms in general.
This article is part of the theme issue ‘Genomic architecture of supergenes: causes and evolutionary consequences’.
Significance
Some social insects exhibit split sex ratios, wherein a subset of colonies produce future queens and others produce males. This phenomenon spawned many influential theoretical studies and empirical tests, both of which have advanced our understanding of parent–offspring conflicts and the maintenance of cooperative breeding. However, previous studies assumed that split sex ratio was not under genetic control. Here, we show that split sex ratio is associated with a large genomic region in two ant species. The discovery that sex allocation can have a genetic basis provides an additional perspective on this well-studied trait of social insects.
The fitness consequences of cooperation can vary across an organism’s lifespan. For non-kin groups, especially, social advantages must balance intrinsic costs of cooperating with non-relatives. In this study, we asked how challenging life history stages can promote stable, long-term alliances among unrelated ant queens. We reared single- and multi-queen colonies of the primary polygynous harvester ant, Pogonomyrmex californicus, from founding through the first ten months of colony growth, when groups face high mortality risks. We found that colonies founded by multiple, unrelated queens experienced significant survival and growth advantages that outlasted the colony founding period. Multi-queen colonies experienced lower mortality than single-queen colonies, and queens in groups experienced lower mortality than solitary queens. Further, multi-queen colonies produced workers at a faster rate than did single-queen colonies, even while experiencing lower per-queen worker production costs. Additionally, we characterized ontogenetic changes in the organization of labor, and observed increasing and decreasing task performance diversity by workers and queens, respectively, as colonies grew. This dynamic task allocation likely reflects a response to the changing role of queens as they are increasingly able to delegate risky and costly tasks to an expanding workforce. Faster worker production in multi-queen colonies may beneficially accelerate this behavioral transition from a vulnerable parent–offspring group to a stable, growing colony. These combined benefits of cooperation may facilitate the retention of multiple unrelated queens in mature colonies despite direct fitness costs, providing insight into the evolutionary drivers of stable associations between unrelated individuals.
Significance
Supergenes are clusters of linked loci producing complex alternative phenotypes. In a series of experiments, we demonstrate that a supergene controlling ant social organization distorts Mendel’s laws to enhance its transmission to adult offspring. One supergene haplotype is specific to multiple-queen colonies. This haplotype kills half of the offspring from heterozygous mothers—all eggs that do not inherit the haplotype fail to hatch. Hence, the haplotype associated with multiple-queen colonies is a selfish genetic element favoring its transmission to the detriment of the alternate haplotype associated with single-queen colonies. Selfish gene drive by a large group of linked genes impacts the social organization of ant colonies, which illustrates the intricate multilevel effects of supergenes.
Supergenes are clusters of linked genetic loci that jointly affect the expression of complex phenotypes, such as social organization. Little is known about the origin and evolution of these intriguing genomic elements. Here we analyse whole-genome sequences of males from native populations of six fire ant species and show that variation in social organization is under the control of a novel supergene haplotype (termed Sb), which evolved by sequential incorporation of three inversions spanning half of a ‘social chromosome’. Two of the inversions interrupt protein-coding genes, resulting in the increased expression of one gene and modest truncation in the primary protein structure of another. All six socially polymorphic species studied harbour the same three inversions, with the single origin of the supergene in their common ancestor inferred by phylogenomic analyses to have occurred half a million years ago. The persistence of Sb along with the ancestral SB haplotype through multiple speciation events provides a striking example of a functionally important trans-species social polymorphism presumably maintained by balancing selection. We found that while recombination between the Sb and SB haplotypes is severely restricted in all species, a low level of gene flux between the haplotypes has occurred following the appearance of the inversions, potentially mitigating the evolutionary degeneration expected at genomic regions that cannot freely recombine. These results provide a detailed picture of the structural genomic innovations involved in the formation of a supergene controlling a complex social phenotype. A supergene controlling social behaviour arose in the common ancestor of six ant species by the sequential incorporation of three inversions.
Nonrecombining genomic variants underlie spectacular social polymorphisms, from bird mating systems to ant social organization. Because these “social supergenes” affect multiple phenotypic traits linked to survival and reproduction, explaining their persistence remains a substantial challenge. Here, we investigate how large nonrecombining genomic variants relate to colony social organization, mating system and dispersal in the Alpine silver ant, Formica selysi. The species has colonies headed by a single queen (monogynous) and colonies headed by multiple queens (polygynous). We confirmed that a supergene with alternate haplotypes—Sm and Sp—underlies this polymorphism in social structure: Females from mature monogynous colonies had the Sm/Sm genotype, while those from polygynous colonies were Sm/Sp and Sp/Sp. Queens heading monogynous colonies were exclusively mated with Sm males. In contrast, queens heading polygynous colonies were mated with Sp males and Sm males. Sm males, which are only produced by monogynous colonies, accounted for 22.9% of the matings with queens from mature polygynous colonies. This asymmetry between social forms in the degree of assortative mating generates unidirectional male‐mediated gene flow from the monogynous to the polygynous social form. Biased gene flow was confirmed by a significantly higher number of private alleles in the polygynous social form. Moreover, heterozygous queens were three times as likely as homozygous queens to be multiply mated. This study reveals that the supergene variants jointly affect social organization and multiple components of the mating system that alter the transmission of the variants and thus influence the dynamics of the system.
Background: Offspring investment strategies vary markedly between and within taxa, and much of this variation is thought to stem from the trade-off between offspring size and number. While producing larger offspring can increase their competitive ability, this often comes at a cost to their colonization ability. This competition–colonization trade- off (CCTO) is thought to be an important mechanism supporting coexistence of alternative strategies in a wide range of taxa. However, the relative importance of an alternative and possibly synergistic mechanism—spatial structuring of the environment—remains the topic of some debate. In this study, we explore the influence of these mechanisms on metacommunity structure using an agent-based model built around variable life-history traits. Our model combines explicit resource competition and spatial dynamics, allowing us to tease-apart the influence of, and explore the interaction between, the CCTO and the spatial structure of the environment. We test our model using two reproductive strategies which represent extremes of the CCTO and are common in ants.
Results: Our simulations show that colonisers outperform competitors in environments subject to higher temporal and spatial heterogeneity and are favoured when agents mature late and invest heavily in reproduction, whereas competitors dominate in low-disturbance, high resource environments and when maintenance costs are low. Varying life-history parameters has a marked influence on coexistence conditions and yields evolutionary stable strategies for both modes of reproduction. Nonetheless, we show that these strategies can coexist over a wide range of life-history and environmental parameter values, and that coexistence can in most cases be explained by a CCTO. By explicitly considering space, we are also able to demonstrate the importance of the interaction between dispersal and landscape structure.
Conclusions: The CCTO permits species employing different reproductive strategies to coexist over a wide range of life-history and environmental parameters, and is likely to be an important factor in structuring ant communities. Our consideration of space highlights the importance of dispersal, which can limit the success of low-dispersers through kin competition, and enhance coexistence conditions for different strategies in spatially structured environments.
Complex adaptive polymorphisms are common in nature, but what mechanisms maintain the underlying favorable allelic combinations [1-4]? The convergent evolution of polymorphic social organization in two independent ant species provides a great opportunity to investigate how genomes evolved under parallel selection. Here, we demonstrate that a large, nonrecombining ''social chromosome'' is associated with social organization in the Alpine silver ant, Formica selysi. This social chromosome shares architectural characteristics with that of the fire ant Solenopsis invicta [2], but the two show no detectable similarity in gene content. The discovery of convergence at two levels - the phenotype and the genetic architecture associated with alternative social forms - points at general genetic mechanisms underlying transitions in social organization. More broadly, our findings are consistent with recent theoretical studies suggesting that suppression of recombination plays a key role in facilitating coordinated shifts in coadapted traits [5, 6].
The hypothesis that obligate eusociality always evolved from ancestral states of strict lifetime monogamy implies that (1) facultatively eusocial lineages had to abandon multifemale breeding to achieve permanent morphologically differentiated castes, and (2) lineages of obligatorily eusocial insects had to independently re-evolve multifemale breeding when that served the inclusive fitness interests of nursing workers. Multiqueen nesting (eusocial polygyny) is known to be common across the ants, but rare in the corbiculate (eusocial) bees, the vespine wasps and the higher termites, but we show that this difference is mostly due to cases of obligate polygyny being restricted to the ants. This pattern is remarkably similar to the distribution of inquiline social parasites that use stealth rather than aggression to invade host colonies, which also repeatedly evolved in ants only. We explore the lineage-specific selection forces that have allowed or constrained de novo evolution of stable eusocial polygyny in Hamiltonian inclusive fitness terms. We argue that perennial life histories, male survival as stored sperm rather than as lifetime mates, and sib competition are possibly sufficient to explain the general prevalence of secondary polygyny across the obligatorily eusocial insects. We infer that obligate polygyny compromises eusocial ‘soma’ and ‘germ-line’ segregation in ways known to decrease developmental stability in metazoans, and we briefly evaluate the selection forces that reduce queen life span in highly, but probably not facultatively, polygynous species. We conclude that secondary polygyny in its obligate (ant) form resembles cooperative breeding with multiple ‘tragedy of the commons’ aspects, but in a peculiar manner because breeding females are selected to exploit the services of unmated workers rather than each other’s. This breeding system has likely been maintained in ants because it allows modular extensions of colonies in directly adjacent habitat of similar quality without the re-emergence of sexual conflicts or unproductive local competition with kin.
Understanding the molecular underpinnings of evolutionary adaptations is a central focus of modern evolutionary biology. Recent studies have uncovered a panoply of complex phenotypes, including locally adapted ecotypes and cryptic morphs, divergent social behaviours in birds and insects, as well as alternative metabolic pathways in plants and fungi, that are regulated by clusters of tightly linked loci. These 'supergenes' segregate as stable polymorphisms within or between natural populations and influence ecologically relevant traits. Some supergenes may span entire chromosomes, because selection for reduced recombination between a supergene and a nearby locus providing additional benefits can lead to locus expansions with dynamics similar to those known for sex chromosomes. In addition to allowing for the co-segregation of adaptive variation within species, supergenes may facilitate the spread of complex phenotypes across species boundaries. Application of new genomic methods is likely to lead to the discovery of many additional supergenes in a broad range of organisms and reveal similar genetic architectures for convergently evolved phenotypes.
Coordination of group actions in social organisms is often a self-organised process lacking central control. These collective behaviours are driven by mechanisms of positive feedback generated through information exchange. Understanding how different methods of communication generate positive feedback is an essential step in comprehending the functional mechanisms underlying complex systems. The Japanese small-colony ant, Myrmecina nipponica uses both pheromone trails and an apparent quorum response during consensus decisions over a new home. Both of these mechanisms have been shown to generate positive feedback and are effective means of selecting among mutually exclusive courses of action. In this study, I investigate how pheromone trails and quorum thresholds contribute to consensus decisions during house-hunting in this species through experimental manipulations of pheromone trails, colony size and environmental context. Results demonstrate that (1) providing colonies with pre-established pheromone trails increased the number of ants finding the new site and led to higher quorum thresholds and more rapid relocations, (2) experimentally halving colony size resulted in a proportional decrease in quorum thresholds and (3) colonies relocating long distances had higher quorums than those relocating short distances. Taken together, these data indicate that pheromone trails are important for recruitment and navigation during nest site selection, but that decision making is contingent on a quorum response. Such synergy between mechanisms of positive feedback may be a common means of optimising collective behaviours.
Stock colonies of five species, Myrmica lobicornis, M. rubra , M. ruginodis, M. scabrinodis, and M. sulcinodis, were collected near Poyakonda (Murmansk district, just on the Polar Circle latitude) at the end of June. Experimental cultures each consisting of 150 workers, one queen and about 100 overwintered larvae were established and maintained in photothermo- static chambers at two temperature regimes - 22.5 or 25°C and three day-lengths - mid-summer photoperiod (24 h), late-August photoperiod (17 h) and autumn photoperiod (12 h). All or almost all larvae pupated regardless of photoperiod and temperature. New larvae emerging from the eggs laid by queens developed up to the third (final) instar and fell in diapause independently of the day-length and temperature. No larvae pupated except for a few in one culture of M. scabrinodis. Thus generally, Myrmica cultures failed to pr oduce so-called rapid brood (i.e. larvae pupated during their first summer) even under long days and optimal temperature. The lack of the photoperiodic control of larval development in th e ant populations stud ied is evidently a consequence of the absence of rapid brood in the colonies. Nevertheless, the photoperiods appeared to control the duration o f oviposition and the time of queen onset of diapause in experiments. It is , h owever, questiona ble that August photoperio ds alone could induce queen diapause in subarctic populations of M. ruginodis in real time. We suppose that queen diapause arises mainly due to the influence of infe rior temperature in August. The possibility of photoperiodic termination of diapause in both queens and larvae in autumn is revealed in all spec ies studied. Fr om this we formulate a new hypothesis of "vestigial photoperiodic responses" in Myrmica populations inhabiting the subarctic regions.
Intraspecific variability in social organization is common, yet the underlying causes are rarely known. In the fire ant Solenopsis invicta, the existence of two divergent forms of social organization is under the control of a single Mendelian genomic element marked by two variants of an odorant-binding protein gene. Here we characterize the genomic region responsible for this important social polymorphism, and show that it is part of a pair of heteromorphic chromosomes that have many of the key properties of sex chromosomes. The two variants, hereafter referred to as the social B and social b (SB and Sb) chromosomes, are characterized by a large region of approximately 13 megabases (55% of the chromosome) in which recombination is completely suppressed between SB and Sb. Recombination seems to occur normally between the SB chromosomes but not between Sb chromosomes because Sb/Sb individuals are non-viable. Genomic comparisons revealed limited differentiation between SB and Sb, and the vast majority of the 616 genes identified in the non-recombining region are present in the two variants. The lack of recombination over more than half of the two heteromorphic social chromosomes can be explained by at least one large inversion of around 9 megabases, and this absence of recombination has led to the accumulation of deleterious mutations, including repetitive elements in the non-recombining region of Sb compared with the homologous region of SB. Importantly, most of the genes with demonstrated expression differences between individuals of the two social forms reside in the non-recombining region. These findings highlight how genomic rearrangements can maintain divergent adaptive social phenotypes involving many genes acting together by locally limiting recombination.
Ant workers are very often reproductively degenerate females, but in some species from subfamily Ponerinae, the workers can mate and lay fertilized eggs just like queens (they are then termed "gamergates"). In Harpegnathos saltator, new colonies are founded independently by single queens, and when senescent they are replaced by several gamergates. This secondary polygyny is distinguished by three features: (1) behavioural data indicate that young workers copulate with their brothers, unlike the queens who disperse and mate outside the nests; (2) gamergate colonies produce both male and female sexuals annually; (3) gamergate colonies appear not to fission. Our evidence for the lack of fission is indirect: the nests of H. saltator are unusually elaborate for ponerine ants, and gamergate colonies produce many young queens (at the expense of investing in workers). Queen supersedure results in an extension of colony lifespan, thus making complex constructions possible with a small colony size (65 ± 40 workers in a western Ghats population; N = 59). In turn, these nests represent a valuable resource to be inherited by successive generations of worker offspring. This life history contrasts with that of other ponerine ants having both queens and gamergates (e.g. in Rhytidoponera confusa, nests are simple and short-lived, gamergates are not inbred and their colonies can fission while producing mostly males; Ward, 1981a, 1983 a).
The spectacular success of eusocial insects can be attributed to their sophisticated cooperation, yet cooperation is conspicuously absent during colony foundation when queens are alone. Selection against this solitary stage has led to a dramatically different strategy in thousands of eusocial insect species in which colonies are started by groups of nestmates and the benefits of sociality are retained continuously. Dependent colony foundation (DCF) evolved recurrently multiple times across the ants, bees, and wasps, though its prevalence in termites remains unclear. We review adaptations at both the colony level (reproductive investment shifts from sexuals to workers) and the individual-level (wingless queens evolve in ants), and other consequences for life history (invasiveness, parasite transmission). Although few studies have focused on DCF, the accumulated data from anecdotal reports, supported by indirect information including morphology, population genetics, and colony demographics, make it clear that this strategy is more diverse and widespread than is usually recognized. Expected final online publication date for the Annual Review of Entomology Volume 58 is December 03, 2013. Please see http://www.annualreviews.org/catalog/pubdates.aspx for revised estimates.
For the past 25 years NIH Image and ImageJ software have been pioneers as open tools for the
analysis of scientific images. We discuss the origins, challenges and solutions of these two programs,
and how their history can serve to advise and inform other software projects.
The reproductive status of individual queens in relation to the number of queens in polygyne colonies of Solenopsis invicta Buren was investigated under both field and laboratory conditions. In field colonies, the weight of individual queens is inversely related to the number of resident queens present. The weight of a queen is positively correlated with fecundity, as measured by the number of eggs laid in 5 h in isolation. Thus increasing queen number has a strong negative effect on the fecundity of individual queens in these colonies. A similar relationship was established in standardized laboratory colonies using queens from a single experimental population. Colony size by itself had no significant effect on queen weight in either the field or laboratory colonies, suggesting that the inverse relationship between queen number and fecundity results from mutual inhibition among queens, possibly involving pheromones, rather than reduced nutrition through lower worker/queen ratios. While uninseminated queens can comprise up to 50% of the functional (i.e. egglaying) queens in polygyne colonies of this ant, they tend to be less fecund than their inseminated nestmates; uninseminated queens within a given colony generally weigh 5–25% less.
To determine whether the production of sexuals in the fire ant, Solenopsis invicta Buren, is related to queen number in the field, the numbers of sexuals in monogyne (M) and polygyne (P) colonies of this species were compared. Large colonies (n=25 M and 25 P) were collected at random during spring, summer and fall when sexuals are actively produced, and the numbers of sexuals present were counted. The numbers of alates plus sexual pupae and larvae in M colonies far exceeded those in P colonies in each season. Significant differences between M and P colonies were also found when the numbers of alates and sexual immatures (pupae + larvae) were compared separately in each season. In addition, M colonies contained significantly more female sexuals (alates + pupae) than did P colonies in the summer and fall, and significantly more males in all three seasons. The negative relationship between queen number and number of sexuals provides evidence that queen control over the production of sexuals, previously established in laboratory experiments, also occurs under natural conditions.
Social organisms vary greatly in the number of breeders per group; yet, the causes and consequences of this variation remain
poorly known. Here, we show that variation in social structure is tightly linked with changes in several fundamental life-history
traits within one population of ants. Multiple-queen colonies of Formica selysi were much more populous than single-queen ones. They also occurred in areas of higher nest density, had longer colony lifespan,
produced smaller queens that presumably disperse less, and invested less in reproductive individuals relative to workers.
These multiple changes in life histories are consistent with a shift in the mode of colony foundation and the degree of philopatry
of queens. They may also provide various fitness benefits to members of multiple-queen colonies and are likely to play a central
role in the evolution and maintenance of polymorphic social structures.
Supergenes, clusters of tightly linked genes, play a key role in the evolution of complex adaptive variation [1, 2]. Although supergenes have been identified in many species, we lack an understanding of their origin, evolution, and persistence [3]. Here, we uncover 20-40 Ma of evolutionary history of a supergene associated with polymorphic social organization in Formica ants [4]. We show that five Formica species exhibit homologous divergent haplotypes spanning 11 Mbp on chromosome 3. Despite the supergene's size, only 142 single nucleotide polymorphisms (SNPs) consistently distinguish alternative supergene haplotypes across all five species. These conserved trans-species SNPs are localized in a small number of disjunct clusters distributed across the supergene. This unexpected pattern of divergence indicates that the Formica supergene does not follow standard models of sex chromosome evolution, in which distinct evolutionary strata reflect an expanding region of suppressed recombination [5]. We propose an alternative "eroded strata model" in which clusters of conserved trans-species SNPs represent functionally important areas maintained by selection in the face of rare recombination between ancestral haplotypes. The comparison of whole-genome sequences across 10 additional Formica species reveals that the most conserved region of the supergene contains a transcription factor essential for motor neuron development in Drosophila [6]. The discovery that a very small portion of this large and ancient supergene harbors conserved trans-species SNPs linked to colony social organization suggests that the ancestral haplotypes have been eroded by recombination, with selection preserving differentiation at one or a few genes generating alternative social organization.
We consider worker-controlled sex investments in eusocial Hymenoptera (ants in particular) and assume that relatedness asymmetry is variable among colonies and that workers are able to assess the relatedness asymmetry in their own colony. We predict that such "assessing" workers should maximize their inclusive fitness by specializing in the production of the sex to which they are relatively most related, i.e., colonies whose workers have a relatedness asymmetry below the population average should specialize in males, whereas colonies whose workers have a higher than average relatedness asymmetry should specialize in making females. Our argument yields the expectation that colony sex ratios will be bimodally distributed in ant populations where relatedness asymmetry is variable owing to multiple mating, worker reproduction, and/or polygyny. No such bimodality is expected, however, in ant species where relatedness asymmetry is known to be constant, or in cases where relatedness asymmetry is supposed to be irrelevant due to allospecific brood rearing under queen control, as in the slave-making ants. Comparative data on colony sex ratios in ants are reviewed to test the predictions. The data partly support our contentions, but are as yet insufficient to be considered as decisive evidence.
Balancing selection describes any form of natural selection which results in the persistence of multiple variants of a trait at intermediate frequencies within populations. By offering up a snapshot of multiple co-occurring functional variants and their interactions, systems under balancing selection can reveal the evolutionary mechanisms favouring the emergence and persistence of adaptive variation in natural populations. We here focus on the mechanisms by which several functional variants for a given trait can arise, a process typically requiring multiple epistatic mutations. We highlight how balancing selection can favour specific features in the genetic architecture and review the evolutionary and molecular mechanisms shaping this architecture. First, balancing selection affects the number of loci underlying differentiated traits and their respective effects. Control by one or few loci favours the persistence of differentiated functional variants by limiting intergenic recombination, or its impact, and may sometimes lead to the evolution of supergenes. Chromosomal rearrangements, particularly inversions, preventing adaptive combinations from being dissociated are increasingly being noted as features of such systems. Similarly, due to the frequency of heterozygotes maintained by balancing selection, dominance may be a key property of adaptive variants. High heterozygosity and limited recombination also influence associated genetic load, since linked recessive deleterious mutations may be sheltered. The capture of deleterious elements in a locus under balancing selection may reinforce polymorphism by further promoting heterozygotes. Finally, according to recent genome-wide scans, balanced polymorphism might be more pervasive than generally thought. We stress the need for both functional and ecological studies to characterize the evolutionary mechanisms operating in these systems. This article is protected by copyright. All rights reserved.
A guide to using S environments to perform statistical analyses providing both an introduction to the use of S and a course in modern statistical methods. The emphasis is on presenting practical problems and full analyses of real data sets.
How polygyny evolved in social insect societies is a long-standing question. This phenomenon, which is functionally similar to communal breeding in vertebrates, occurs when several queens come together in the same nest to lay eggs that are raised by workers. As a consequence, polygyny drastically reduces genetic relatedness among nestmates. It has been suggested that the short-term benefits procured by group living may outweigh the costs of sharing the same nesting site and thus contribute to organisms rearing unrelated individuals. However, tests of this hypothesis are still limited. To examine the evolutionary emergence of polygyny, we reviewed the literature to build a data set containing life-history traits for 149 Palearctic ant species and combined this data set with a reconstructed phylogeny. We show that monogyny is the ancestral state and that polygyny has evolved secondarily and independently throughout the phylogenetic tree. The occurrence of polygyny is significantly correlated with larger colony size, dependent colony founding and ecological dominance. Although polydomy (when a colony simultaneously uses several connected nests) tends to occur more frequently in polygynous species, this trend is not significant when phylogenetic history is accounted for. Overall, our results indicate that polygyny may have evolved in ants in spite of the reduction in nestmate relatedness because large colony size provides immediate ecological advantages, such as the more efficient use of temporal food resources. We suggest that the competitive context of ant communities may have provided the conditions necessary for the evolution of polygyny in some clades.
This is the first compilation of our research and data from the literature on the duration and thermal reaction norms for development in ants. Altogether, 97 regression lines characterizing the linear dependence of ant brood (egg, larval, prepupal and pupal) development on temperature were obtained for 33 species from 15 genera and three subfamilies. Significant positive correlations between the durations of different immature stages were revealed. We found differences between thermal reaction norms for development for various immature stages, some taxonomic groups, and southern and northern groups of species. All immature stages appeared to be shorter on average at 25°C in northern ants compared to southern species; this difference is insignificant only for eggs. Highly significant negative correlations were revealed between the temperature threshold for development (TTD) and the sum of degree-days (SDD) for all immature stages. The latitudinal trends in intraspecific variation of thermal constants appeared to be opposite to those we observed at the interspecific level. At the latter, the coefficient of thermal sensitivity of development (i.e. the coefficient of linear regression of development rate on temperature) and TTD tends to decrease and SDD to increase from the south to the north. In contrast, at the intraspecific level, development became more temperature-sensitive in northern populations, i.e. characterized by higher slopes of regression lines of development rate on temperature, and higher TTDs. The species of the genus Formica are characterized by the shortest and the most temperature-sensitive immature development among all the ant species studied.
Individuals within social groups often show consistent differences in behaviour across time and context. Such interindividual differences and the evolutionary challenge they present have recently generated considerable interest. Social insects provide some of the most familiar and spectacular examples of social groups with large interindividual differences. Investigating these within-group differences has a long research tradition, and behavioural variability among the workers of a colony is increasingly regarded as fundamental for a key feature of social insects: division of labour. The goal of this review is to illustrate what we know about both the proximate mechanisms underlying behavioural variability among the workers of a colony and its ultimate consequences; and to highlight the many open questions in this research field. We begin by reviewing the literature on mechanisms that potentially introduce, maintain, and adjust the behavioural differentiation among workers. We highlight the fact that so far, most studies have focused on behavioural variability based on genetic variability, provided by e.g. multiple mating of the queen, while other mechanisms that may be responsible for the behavioural differentiation among workers have been largely neglected. These include maturational, nutritional and environmental influences. We further discuss how feedback provided by the social environment and learning and experience of adult workers provides potent and little-explored sources of differentiation. In a second part, we address what is known about the potential benefits and costs of increased behavioural variability within the workers of a colony. We argue that all studies documenting a benefit of variability so far have done so by manipulating genetic variability, and that a direct test of the effect of behavioural variability on colony productivity has yet to be provided. We emphasize that the costs associated with interindividual variability have been largely overlooked, and that a better knowledge of the cost/benefit balance of behavioural variability is crucial for our understanding of the evolution of the mechanisms underlying the social organization of insect societies. We conclude by highlighting what we believe to be promising but little-explored avenues for future research on how within-colony variability has evolved and is maintained. We emphasize the need for comparative studies and point out that, so far, most studies on interindividual variability have focused on variability in individual response thresholds, while the significance of variability in other parameters of individual response, such as probability and intensity of the response, has been largely overlooked. We propose that these parameters have important consequences for the colony response. Much more research is needed to understand if and how interindividual variability is modulated in order to benefit division of labour, homeostasis and ultimately colony fitness in social insects.
Split sex ratio theory is an important extension of sex allocation
theory. It suggests that colony sex ratios in social insects vary
because workers control sex allocation and respond to variations in
their comparative relatedness with females and males (relatedness
asymmetry). In a population of the ant Leptothorax acervorum, 21
monogynous (single-queen) colonies produced a female-biased sex ratio
(62% females), and 24 polygynous (multiple-queen) colonies produced a
male-biased sex ratio (28% females). Within the polygynous colonies,
queen number did not affect sex ratio (with colony productivity
statistically controlled). As colony productivity rose, the sex ration
either did not change (monogynous colonies) or became more male-biased
(polygynous colonies). The fraction invested in sexuals rose with
increasing colony size and productivity in monogynous but not in
polygynous colonies, which invested less in sexuals. These findings
suggest that split sex ratios in L. acervorum stem from two processes.
The first is workers' response to the variation in relatedness asymmetry
caused by variable queen numbers. The second is sexratio compensation by
monogynous colonies for male-biased production in polygynous colonies.
This arises because polygynous colonies reproduce, partly, by colony
budding and so have daughter colonies subject to local resource
competition.
In ants, there are two main strategies of colony founding: young queens can start colonies without the help of workers (independent mode), or young queens need the help of workers (dependent mode). Independent founding is generally assumed to be the common manner of colony founding in ants, whereas dependent founding is thought to be a derived character typical of polygyne (i.e., several queens per colony) species with unicolonial nests.A comparative study of 24 European ant species showed that dependent colony founding is not restricted to unicolonial polygyne species but that a significant proportion of all polygyne species utilize this mode of reproduction. Twelve (92%) of 13 monogyne (i.e., a single queen per colony) species were independent founding species, and only one (8%) employed budding. In contrast, only three (27%) of the 11 polygyne species always used independent founding, two (18%) were either independent or dependent founding species, five (45%) of them employed only budding and one (9%) parasitic founding, suggesting that mode of colony founding may be associated with queen number per colony. Additionally, queen number per colony correlates with mode of colony founding in eight pairs (from seven different genera and four subfamilies) of closely related species (or forms) with contrasting modes of colony founding. In seven pairs, the independent founding species or form is monogyne, whereas its counterpart using budding is polygyne. In one additional pair, both forms are polygyne, but the form using dependent founding exhibits a higher degree of polygyny.Differences in the manner species start new colonies must influence the probability that newly-mated queens survive and successfully reproduce, and therefore the mode of reproduction should be considered when comparing reproductive success of queens across species. This is especially true since the present study shows that even closely related species can frequently differ in their mode of colony founding.
We present an inclusive fitness model on worker-controlled sex investments in eusocial Hymenoptera which expands the existing theory for random mating populations as formulated by Trivers and Hare (1976) and Benford (1978). We assume that relatedness asymmetry is variable among colonies — owing to multiple mating, worker reproduction and polygyny — and that workers are able to assess the relatedness asymmetry in their own colony. A simple marginal value argument shows that “assessing” workers maximize their inclusive fitness by specializing on the production of the sex to which they are relatively more related than the average worker in the population is related to that sex. The model confirms our earlier verbal argument on this matter (Boomsma and Grafen, 1990) and gives further quantitative predictions of the optimal sex ratio of relatedness-asymmetry classes for both infinite and finite, random mating populations.
It is shown that in large populations all but one of the relatedness-asymmetry classes should specialize on the production of one sex only. The remaining, balancing class is selected to compensate any bias induced by the other class(es) such that the population sex ratio reflects the relatedness asymmetry of that balancing class. In the absence of worker-reproduction, the sex ratio compensation by the balancing-class is generally close to 100%, unless the population is very small.
In the Discussion we address explicitly the likelihood of our relatedness-assessment hypothesis and other assumptions made in the model. The relationship of our model with previous theory on sex allocation in eusocial Hymenoptera is worked out in the Appendix.
In this landmark volume, an international group of scientists has synthesized their collective expertise and insight into a newly unified vision of insect societies and what they can reveal about how sociality has arisen as an evolutionary strategy.Jürgen Gadau and Jennifer Fewell have assembled leading researchers from the fields of molecular biology, evolutionary genetics, neurophysiology, behavioral ecology, and evolutionary theory to reexamine the question of sociality in insects. Recent advances in social complexity theory and the sequencing of the honeybee genome ensure that this book will be valued by anyone working on sociality in insects. At the same time, the theoretical ideas presented will be of broad-ranging significance to those interested in social evolution and complex systems.
In a survey for multiple-queen colonies of the fire ant, Solenopsis invicta Buren, 15 colonies were found in Mississippi, but none could be found in Georgia. The 15 contained 476 dealated females (3–63 per colony) of which 87% were shown, partly by direct observation but chiefly by means of oviposition tests, to be functional egg-layers. Dissection of 133 of these females showed that 96% had mature oocytes in their ovarioles and 90% were inseminated.
All the queens of the 15 polygynous colonies were less physogastric than queens of monogynous colonies, and individually they laid far fewer eggs, but collectively they produced a significantly greater number of eggs per colony. The significance of polygyny in the North American populations of S. invicta is briefly discussed.
1. Myrmecina nipponica has two types of colonies: a queen colony type, in which the reproductive females are queens and new colonies are made by independent founding, and an intermorphic female colony type, in which reproductive females belong to a wingless intermediate morphology between queen and worker, and where colonies multiply through colonial budding.
2. The mating frequencies of reproductive females in both types indicate monoandry. The relatedness among nestmates in both types was almost 0.75, however relatedness between mother and daughter in intermorphic female colonies was slightly higher than that of queen colonies.
3. The sex ratio (corrected investment female ratio) was 0.70 at the population level, suggesting that the sex ratio is controlled by workers in this species, however the ratio differed greatly between the two types of colonies. Queen colonies (n = 37) had a female-biased sex ratio of 0.77 while intermorphic female colonies (n = 33) had a ratio of 0.56.
4. Each reproductive intermorphic female was accompanied by an average of 2.9 workers (including virgin intermorphic females) in the colonial budding, and when the investment to those workers was added to the female investment, the sex ratio reached 0.81.
5. The frequency distribution of sex ratio was bimodal, with many colonies producing exclusively males or females, however mean estimated relatedness within colonies was almost 0.75. These data are inconsistent with the genetic variation hypothesis, which is one of the predominant hypotheses accounting for the between-colony variation in sex ratio.
The pervasive social and ecological differences between ant colonies that have a single queen and those that have multiple queens are defined. The evolutionary tendencies which lead to polygyny and the adaptive significance of multiple queens are examined. The discussion of the ecological consequences of polygyny and monogyny leads to a deeper understanding of territoriality, spacing and species packing in ants.
Queen/worker thorax volume ratios were calculated in nine monogynous, seven polygynous and eight parasitic ant species in order to determine whether mode of nest founding is reflected in relative gyne size. A significant difference in this ratio was found between monogynous (independent nest founders) and polygynous and parasitic species (dependent nest founders). Thorax volume ratio in ants appears to be independent of actual gyne or worker size and can be used as a relative measure sure of colony investment in the gynes. Furthermore, thorax volume ratio seems to reflect the mode of nestfounding behaviour when compared between species within genera as well as among species in general. Polygyny is discussed as a nest-founding strategy that is selected for when nest founding by single gynes is difficult and costly. In addition, secondary benefits could be gained by polygynous colonies since investment in gyne size could be decreased.
There is high within-nest relatedness for functional queens (with corpora lutea), nonfunctional queens (without corpora lutea), and workers in polygynous nests of Leptothorax acervorum. The high functional queen relatedness suggests that young mated queens are adopted back to their mother nest. Functional queen relatedness does not change with the number of queens present in the nest, suggesting that the number of generations of queens, on average two to three, is rather stable. Worker relatedness decreases with increasing number of functional queens per nest (Tables 5, 6). The number of queens contributing offspring to the nest (mothers), estimated from worker and functional queen relatedness, is lower than the number of functional queens, particularly in highly polygynous nests. Estimates of number of mothers in monogynous nests indicate that these nests previously were polygynous (Table 7). There is no correlation between nest relatedness and distance between nests, and budding-off, if present, thus appears to be a rare mode of nest founding (Table 8). There are no indications of inbreeding in the two populations studied since the frequency of heterozygotes is as high as expected from random mating (Table 4). Most likely, polygyny is the rule in L. acervorum and serves to secure the presence of queens in the nest.
Sexual behavior of Myrmecina graminicola in laboratory conditions is described. Virgin females, both gynomorphs and intermorphs, exhibit an inconspicuous "sexual calling", apparently depositing a sex pheromone on the substrate close by. The sexual pheromone is produced in the poison gland. Copulation needs between 40 and 60 seconds, dealation of gynomorphs follows soon after. Some observations are in marked contrast to former reports, e.g. on duration of copulation in M. graminicola (Donisthorpe, 1927: several hours) and on the source of a sex pheromone in the closely related M. nipponica (Murakami et al., 2002: pygidial gland).
Summary: Polymorphism of the functional queens in Myrmecina graminicola is analyzed. Both gynomorphs (G-§ G) and a wide range of intermorphs (I-§ I) occur, which all are usually mated and egg-laying. Colonies having a gynomorphic queen are always monogynous, whereas about 57% of all colonies with intermorphic queens are polygynous, having two or more coexisting functional queens. The female sexual offspring of individual gynomorphic queens either consists of gynomorphs only, or exclusively of intermorphs. Intermorphic queens may have exclusively intermorphic female sexual progeny, or simultaneously both gynomorphs and intermorphs. Single colonies in laboratory culture produce the same kind of female progeny over several subsequent breeding cycles (artificially compressed "years" of 9-10 months). No environmental influence on queen morph determination could be detected. A genetically mediated queen polymorphism, as in Harpagoxenus sublaevis and Leptothorax sp. A, is suggested. Colony sizes vary considerably, with polygynous I-queen colonies being largest (57.2 - 34.3 s.d. workers), followed by G-queen colonies (44.6 - 22.7 s.d.) and monogynous I-queen colonies (34.4 - 23.7 s.d.), suggesting occasional budding of polygynous colonies.
We investigated the process of sexual maturation in winged queens of the fire ant Solenopsis invicta, a species with two distinct forms of social organization. We found that queens of the monogynous social form (single reproductive queen per colony) differ little or not at all from queens of the polygynous form (multiple reproductive queens per colony) in weight and fat content when these are pupae or newly-eclosed adults. Furthermore, the size of a sclerotized region of the adult thorax, which is set during larval growth, does not differ between queens of the two forms. In contrast, winged queens of the two social forms differ dramatically in their physiological phenotypes once they have matured, with monogynous queens weighing more and having greater fat reserves than polygynous queens. A crossfostering experiment revealed that the different maturation processes of queens of the two forms are induced largely by the type of colony in which a queen matures (monogynous or polygynous) rather than being due to intrinsic genetic differences between the forms. However, genetic variation at a single locus does appear to play some role in determining physiological phenotype in queens of the polygynous form, providing an example of genotype-environment interaction in the expression of these physiological traits. Differences between the social forms in the mature phenotypes that are produced constrain the reproductive options of queens, so that the characteristic social organization of a colony is perpetuated by virtue of the social environment in which new queens are reared.
The change over time in the fecundity and weight of queens was investigated in three monogynous, independent colony founding species,Lasius niger, Camponotus ligniperda andC. herculaneus, and two polygynous dependent colony founding species,Plagiolepis pygmaea andIridomyrmex humilis. Queens of the three species founding independently exhibited a similar pattern with a significant loss of weight between mating and the emergence of the first workers. In contrast, weights of queens of the species employing dependent colony founding remained more stable. Fecundity of queens founding independently increased slowly with time whereas fecundity of queens founding dependently reached the maximum level some weeks after the beginning of the first reproductive season. These results are discussed in relation to some differences in the life history (e.g., life-span) between queens utilizing independent and dependent colony founding.On a tud dans ce travail les variations en fonction du temps de la fcondit et du poids des reines fondatrices de trois espces monogynes fondation indpendante (Lasius niger, Camponotus ligniperda, Camponotus herculeanus) et de deux espces polygynes fondation dpendante (Plagiolepis pygmaea etIridomyrmex humilis). Les reines fondatrices des trois espces fondation indpendante montrent des similitudes avec une perte de poids significative entre le moment de l'accouplement et celui de l'mergence des premires ouvrires. A l'inverse, le poids des jeunes reines fondation dpendante reste plus stable aprs l'accouplement. La fcondit des reines fondant de manire indpendante augmente lentement avec le temps, alors que celle des reines fondant de faon dpendante atteint son niveau maximal quelques semaines seulement aprs le dbut de la premire saison d'activit. Ces rsultats sont discuts dans le cadre des diffrences phnologiques (comme par exemple l'esprance de vie) qui apparaissent entre les reines pratiquant les deux types de fondation.
In ants, there are two main processes of colony founding, the independent and the dependent modes. In the first case young queens start colony founding without the help of workers, whereas in the second case they are accompanied by workers. To determine the relation between the mode of colony founding and the physiology of queens, we collected mature gynes of 24 ant species. Mature gynes of species utilizing independent colony founding had a far higher relative fat content than gynes of species employing dependent colony founding. These fat reserves are stored during the period of maturation, i.e. between the time of emergence and mating, and serve as fuel during the time of colony founding to nurture the queen and the brood. Gynes of species founding independently but non claustrally were found to have a relative fat content intermediate between the values found for gynes founding independently and those founding dependently. This suggests that such gynes rely partially on their fat reserves and partially on the energy provided by prey they collect to nurture themselves and the first brood during the time of colony founding. Study of the fat content of mature gynes of all species has shown that it gives a good indication of the mode of colony founding.
In the ant Cardiocondyla obscurior, wingless males compete with nestmate males for access to female mating partners, leading to local mate competition (LMC). Queen number varies between colonies, resulting in variation in the strength of LMC. Cremer & Heinze (2002, Proceedings of the Royal Society of London, Series B, 269, 417–422) showed that colonies responded to increasing queen number by producing a less female-biased sex ratio, as predicted by LMC theory. However, the proximate mechanisms responsible for this variation in the sex ratio could not be determined because the study was restricted to adult sex ratios. With LMC, the primary sex ratio (proportion of haploid eggs laid by the queen) is expected to be female biased, which lowers the conflict between queens and workers over sex allocation. We compared the primary sex ratios laid by queens in monogynous and in polygynous experimental colonies of C. obscurior. The proportion of haploid eggs laid by queens was significantly lower in single-queen than in multiple-queen colonies. Furthermore, queens rapidly adjusted their primary sex ratios to changes in colony queen number. This is the first report of an adaptive adjustment of the primary sex ratio in response to LMC by ant queens.