No mate preference associated with the supergene controlling social organization in Alpine silver ants

Disassortative mating is a powerful mechanism stabilizing polymorphisms at sex chromosomes and other supergenes. The Alpine silver ant, Formica selysi, has two forms of social organization—single‐queen and multiple‐queen colonies—determined by alternate haplotypes at a large supergene. Here, we explore whether mate preference contributes to the maintenance of the genetic polymorphism at the social supergene. With mate choice experiments, we found that females and males mated randomly with respect to social form. Moreover, queens were able to produce offspring irrespective of whether they had mated with a male from the same or the alternative social form. Yet, females originating from single‐queen colonies were more fertile, suggesting that they may be more successful at independent colony founding. We conclude that the pattern of asymmetric assortative mating documented from mature F. selysi colonies in the field is not caused by mate preferences or major genetic incompatibilities between social forms. More generally, we found no evidence that disassortative mate preference contributes to the maintenance of polymorphism at this supergene controlling ant social organization.     

Male reproductive fitness and queen polyandry are linked to variation in the supergene Gp-9 in the fire ant Solenopsis invicta

Supergenes are clusters of tightly linked loci maintained in specific allelic combinations to facilitate co-segregation of genes governing adaptive phenotypes. In species where strong selection potentially operates at different levels (e.g. eusocial Hymenoptera), positive selection acting within a population to maintain specific allelic combinations in supergenes may have unexpected consequences for some individuals, including the preservation of disadvantageous traits. The nuclear gene Gp-9 in the invasive fire ant Solenopsis invicta is part of a non-recombining, polymorphic supergene region associated with polymorphism in social organization as well as traits affecting physiology, fecundity and behaviour. We show that both male reproductive success and facultative polyandry in queens have a simple genetic basis and are dependent on male Gp-9 genotype. Gp-9(b) males are unable to maintain exclusive reproductive control over their mates such that queens mated to Gp-9(b) males remain highly receptive to remating. Queens mated to multiple Gp-9(B) males are rare. This difference appears to be independent of mating plug production in fertile males of each Gp-9 genotype. However, Gp-9(b) males have significantly lower sperm counts than Gp-9(B) males, which could be a cue to females to seek additional mates. Despite the reduced fitness of Gp-9(b) males, polygyne worker-induced selective mortality of sexuals lacking b-like alleles coupled with the overall success of the polygyne social form act to maintain the Gp-9(b) allele within nature. Our findings highlight how strong worker-induced selection acting to maintain the Gp-9(b) allele in the polygyne social form may simultaneously result in reduced reproductive fitness for individual sexual offspring.     

The fire ant social chromosome supergene variant Sb shows low diversity but high divergence from SB

Variation in social behaviour is common, yet little is known about the genetic architectures underpinning its evolution. A rare exception is in the fire ant Solenopsis invicta: Alternative variants of a supergene region determine whether a colony will have exactly one or up to dozens of queens. The two variants of this region are carried by a pair of ‘social chromosomes’, SB and Sb, which resemble a pair of sex chromosomes. Recombination is suppressed between the two chromosomes in the supergene region. While the X‐like SB can recombine with itself in SB/SB queens, recombination is effectively absent in the Y‐like Sb because Sb/Sb queens die before reproducing. Here, we analyse whole‐genome sequences of eight haploid SB males and eight haploid Sb males. We find extensive SB–Sb differentiation throughout the >19‐Mb‐long supergene region. We find no evidence of ‘evolutionary strata’ with different levels of divergence comparable to those reported in several sex chromosomes. A high proportion of substitutions between the SB and Sb haplotypes are nonsynonymous, suggesting inefficacy of purifying selection in Sb sequences, similar to that for Y‐linked sequences in XY systems. Finally, we show that the Sb haplotype of the supergene region has 635‐fold less nucleotide diversity than the rest of the genome. We discuss how this reduction could be due to a recent selective sweep affecting Sb specifically or associated with a population bottleneck during the invasion of North America by the sampled population.     

The fire ant social supergene is characterized by extensive gene and transposable element copy number variation

In the fire ant Solenopsis invicta, a supergene composed of ~600 genes and having two variants, SB and Sb, regulates colony social form. In single queen colonies, all individuals carry only the SB allele, while in multiple queen colonies, some individuals carry the Sb allele. In this study, we characterized genes with copy number variation between SB and Sb‐carrying individuals. We showed extensive acquisition of gene duplicates in the Sb genome, with some likely involved in polygyne‐related phenotypes. We found 260 genes with copy number differences between SB and Sb, of which 239 have greater copy number in Sb. We observed transposable element (TE) accumulation on Sb, likely due to the accumulation of repetitive elements on the nonrecombining chromosome. We found a weak correlation between TE copy number and differential expression, suggesting some TEs may still be proliferating in Sb while many of the duplicated TEs have presumably been silenced. Among the 115 non‐TE genes with higher copy in Sb, enzymes responsible for cuticular hydrocarbon synthesis were highly represented. These include a desaturase and an elongase, both potentially responsible for differential queen odour and likely beneficial for polygyne ants. These genes seem to have translocated into the supergene from other chromosomes and proliferated by multiple duplication events. While the presence of TEs in supergenes is well documented, little is known about duplication of non‐TE genes and their possible adaptive role. Overall, our results suggest that gene duplications may be an important factor leading to monogyne and polygyne ant societies.     

Investigation of the population genetic structure and mating system in the ant Pheidole pallidula

The origin of eusociality in haplo-diploid organisms such as Hymenoptera has been mostly explained by kin selection. However, several studies have uncovered decreased relatedness values within colonies, resulting primarily from multiple queen matings (polyandry) and/or from the presence of more than one functional queen (polygyny). Here, we report on the use of microsatellite data for the investigation of sociogenetic parameters, such as relatedness, and levels of polygyny and polyandry, in the ant Pheidole pallidula. We demonstrate, through analysis of mother-offspring combinations and the use of direct sperm typing, that each queen is inseminated by a single male. The inbreeding coefficient within colonies and the levels of relatedness between the queens and their mate are not significantly different from zero, indicating that matings occur between unrelated individuals. Analyses of worker genotypes demonstrate that 38% of the colonies are polygynous with 2-4 functional queens, and suggest the existence of reproductive skew, i.e. unequal respective contribution of queens to reproduction. Finally, our analyses indicate that colonies are genetically differentiated and form a population exhibiting significant isolation-by-distance, suggesting that some colonies originate through budding.     

Queen mating and paternity variation in the ant Lasius niger

We have electrophoretically analysed the variation in queen mating and worker paternity across and within seven populations of the ant Lasius niger in northwestern Europe. Populations were panmictic and not genetically differentiated ( F _ST = 0.003 ± 0.004; range c. 1000 km). Queens ( n = 535) were shown to mostly mate with a single male, but double mating occurred in all populations and triple mating was found in one case (the total number of worker offspring analysed for paternity was 4825). The genetically effective queen mating frequency was 1.16 on average across populations (range 1.04–1.42). Double sampling of six out of the seven populations showed that most of the variation in queen mating occurred among populations and not within populations among years. Also, paternity skew in colonies with double-mated queens was relatively constant per site but varied across populations. Paternity skew was high in populations with low frequencies of double queen-mating, low in populations with intermediate frequencies of double queen mating and ambiguous in a single population where more than half of the queens mated multiply. Double-mated queens were only collected halfway through a nuptial flight, suggesting that double mating is time consuming and that the mating swarm sex ratio may affect the likelihood of multiple mating towards the end of a flight. No difference in fresh weight between single- and double-mated queens from the same population was found.     

Convergence of genotypic frequencies for differential selfing and positive assortative mating at a biallelic locus

For a biallelic model of differential self-fertilization and differential positive assortative mating based on genotype, it is shown that the genotypic frequencies converge for all sets of mating system parameters. Overdominance and underdominance with respect to the parameters are necessary but not sufficient conditions for global convergence to a polymorphic equilibrium and local attractiveness of both the fixation states, respectively. There are cases of overdominance and underdominance for which one fixation state is globally attractive. The relationship of the result to those known from the classical viability selection model are briefly discussed. For the multiallelic version, it is shown that after the first generation all of the homozygote frequencies are always in excess of the corresponding Hardy-Weinberg proportions if at least one homozygote rate of self-fertilization or assortment probability is positive.     

A new interpretation of the social organization and mating system of the Callitrichidae

Tamarins and marmosets are usually described as monogamous, or as living in extended family groups. Field research on a variety of callitrichid species shows, however, that immigration and emigration by adults are common and that groups are likely to be composed largely of unrelated adults of both sexes. Despite the number of adult females present in a group, only a single female is usually reproductively active. This female may mate with more than one male. Care for the young is provided by all group members but principally by adult males. This generally is referred to as a “communal breeding system. ” However, a vertebrate social system in which more than two reproductively active adults participate in infant care is rare and has otherwise been reported only in a small number of avian and canid species. Wild callitrichid groups virtually always include helpers, but the number of adults of each sex is highly variable. We propose that the Callitrichidae tend to live in small multimalemultifemale groups, communally rear the young of one female, and exhibit a mating pattern characterized by female promiscuity but a breeding system that is functionally polyandrous. There is a significant correlation between the number of males and a group and the total number of surviving young. The possible adaptive advantages of this social organization are discussed. An erratum to this article is available at .     

Population structure and mating biology of the polygynous ponerine ant Gnamptogenys striatula in Brazil

Gnamptogenys striatula is a polygynous ponerine ant, whose colonies contain either several differentiated queens or several gamergates. Population structure, queen mating frequency and deviation from random mating were investigated in a north-eastern Brazilian population. Eight workers from each of 33 queenright colonies and 17 queens and their progeny (20-40 offspring) were genotyped using eight variable microsatellite markers. Population differentiation tests indicated limited gene flow at the scale of several kilometres, and tests of isolation by distance revealed population viscosity at the scale of a few metres. This population structure, together with the frequent colony migrations and fissions observed in the field, suggest that new nests are founded by budding in G. striatula. Genetic data showed that 13 of our 17 queens were single-mated and four were double-mated. The estimation of the range of maximal frequency of double-mated queens in the population was 0.232-0.259, demonstrating that mating frequency is low in G. striatula. The low estimated mean relatedness between the 17 queens and their mates (-0. 04 +/- 0.49) indicated no evidence of inbreeding in G. striatula.     

Mating frequency and mating system of the polygynous ant, Leptothorax acervorum

Multiple mating by queens (polyandry) and the occurrence of multiple queens in the same colony (polygyny) alter patterns of relatedness within societies of eusocial insects. This is predicted to influence kin-selected conflicts over reproduction. We investigated the mating system of a facultatively polygynous UK population of the ant Leptothorax acervorum using up to six microsatellite loci. We estimated mating frequency by genotyping 79 dealate (colony) queens and the contents of their sperm receptacles and by detailed genetic analysis of 11 monogynous (single-queen) and nine polygynous colonies. Results indicated that 95% of queens were singly mated and 5% of queens were doubly mated. The corrected population mean mating frequency was 1.06. Parentage analysis of adults and brood in 17 colonies (10 monogynous, 7 polygynous) showed that female offspring attributable to each of 31 queens were full sisters, confirming that queens typically mate once. Inbreeding coefficients, queen-mate relatedness of zero and the low incidence of diploid males provided evidence that L. acervorum sexuals mate entirely or almost entirely at random. Males mated to queens in the same polygynous colony were not related to one another. Our data also confirmed that polygynous colonies contain queens that are related on average and that their workers had a mixed maternity. We conclude that the mating system of L. acervorum involves queens that mate near nests with unrelated males and then seek readoption by those nests, and queens that mate in mating aggregations away from nests, also with unrelated males.     

Sexual selection and assortative mating by size and their roles in the maintenance of a polymorphism in Swedish Littorina saxatilis populations

Two independent components of mating behaviour, sexual selection and assortative mating, were studied in two allopatric morphs, one sheltered boulder shore form (S-morph) and one exposed cliff shore form (E-morph), of Littorina saxatilis from the west coast of Sweden. Sexual selection was studied by comparing the sizes of copulating and non-copulating snails in the field. Size assortative mating was studied by collecting copulating pairs in the field, while assortative mating between morphs was investigated by bringing the pure morphs together in intermediary habitats and then noting the matings. The S-morph mated randomly in relation to size in two of the studied populations and exhibited a trend towards size assortative mating in a third, while the E-morph showed size assortative mating in both studied populations. The microdistribution of sizes of snails on the shores could not explain all the size assortative mating found, and instead it is argued that a size-based mate rejection behaviour also contributes to the assortative mating in at least some of these populations. There was sexual selection on size in both males and females in the S-morph, with large individuals being favoured as mates. In contrast, copulating snails of the E-morph were smaller than non-copulating ones. The significantly different sexual selection intensities between the two morphs may help to explain the size differences between them. There was random mating between the E- and the S-morphs of L. saxatilis, which suggests no incipient reproductive isolation between morphs on Swedish rocky shores. This is in agreement with earlier studies of Swedish populations, but is in contrast to the situation found in other geographical areas.     

Cuticular profiles and mating preference in a slave-making ant

The remarkable ability of slave-making ants to integrate chemically in the colonies of their host species makes them useful model systems for investigating the role of cuticular hydrocarbons in chemical recognition. The purpose of our study was to examine the influence of the rearing host species on the cuticular hydrocarbon profile and on the mating behaviour of sexuals of the slave-making ant Chalepoxenus muellerianus. Sexuals from a population parasitizing exclusively the host species Temnothorax unifasciatus were reared in the laboratory either with their natural host or another potential host species, Temnothorax recedens. C. muellerianus males reared with T. unifasciatus investigated and mounted female sexuals reared with the same host significantly more often than female sexuals reared with T. recedens. Similarly, C. muellerianus males reared with T. unifasciatus discriminated against female sexuals from natural T. recedens colonies. Males experimentally or naturally reared with T. recedens did not clearly discriminate between female sexuals reared by the two host species and only rarely engaged in mating attempts with either type of female sexuals. Chemical analyses showed that host species affect the chemical profile of C. muellerianus sexuals and vice versa. Our findings indicate that cuticular hydrocarbons might be important in the mating success of this ant species. Received 21 June 2006; revised 20 February 2007; accepted 1 March 2007.     

Genetic divergence and assortative mating between colour morphs of the sea urchin Paracentrotus gaimardi

Some species of sea urchins feature large variation in pigmentation. This variability may be the result of phenotypic plasticity or it may be associated with genetic divergence between morphs. Paracentrotus gaimardi exhibits five colour morphs (pink, brown, green, grey and black), which often occur side by side on the same rock. We studied genetic divergence between these morphs in three populations on the coast of Brazil. A fragment of the region encoding the mitochondrial ATPase 8 and 6 mitochondrial genes, a fragment of the intron of a nuclear histone and the entire nuclear gene coding for the sperm protein bindin were analysed. Mitochondrial DNA was differentiated between the pink and all other morphs, but the histone intron was similar in all colour morphs. In bindin, nine codons were found to be under positive selection and significant differences of allelic frequencies were observed in almost all pairwise comparisons between colour morphs. Although the molecular differentiation in bindin is not large enough to suggest reproductive isolation, some degree of assortative mating within morphs seems to be occurring in this species.     

Effects of social organization and elevation on spatial genetic structure in a montane ant

Studying patterns of population structure across the landscape sheds light on dispersal and demographic processes, which helps to inform conservation decisions. Here, we study how social organization and landscape factors affect spatial patterns of genetic differentiation in an ant species living in mountainous regions. Using genome‐wide SNP markers, we assess population structure in the Alpine silver ant, Formica selysi. This species has two social forms controlled by a supergene. The monogyne form has one queen per colony, while the polygyne form has multiple queens per colony. The two social forms co‐occur in the same populations. For both social forms, we found a strong pattern of isolation‐by‐distance across the Alps. Within regions, genetic differentiation between populations was weaker for the monogyne form than for the polygyne form. We suggest that this pattern is due to higher dispersal and effective population sizes in the monogyne form. In addition, we found stronger isolation‐by‐distance and lower genetic diversity in high elevation populations, compared to lowland populations, suggesting that gene flow between F. selysi populations in the Alps occurs mostly through riparian corridors along lowland valleys. Overall, this survey highlights the need to consider intraspecific polymorphisms when assessing population connectivity and calls for special attention to the conservation of lowland habitats in mountain regions.     

Evolution of ungulate mating systems: Integrating social and environmental factors

Ungulates exhibit diverse mating systems that range from monogamous pair territories to highly polygynous leks. We review mating systems and behaviors across ungulates and offer a new approach synthesizing how interacting factors may shape those mating systems. Variability exists in mating systems among and within species of ungulates and likely is affected by predation risk, availability of resources (food and mates), habitat structure, and sociality. Ungulate mating systems may be labile as a consequence of the varying strength of those interacting factors. In addition, degree of polygyny and sexual dimorphism in size are associated with the evolution of mating systems. Neither male–male combat nor paternal care, however, can completely explain differences in sexual size dimorphism for ungulates, a necessary component in understanding the development of some mating systems. Whatever the evolutionary pathway, sexual segregation limits paternal care allowing more intense male–male competition. Selection of habitat structure, because it modifies risk of predation, is a major determinant of sociality for ungulates. Likewise, ruggedness and steepness of terrain limit the types of mating systems that can occur because of limitations in group size and cohesiveness, as well as the ability of males to herd even small groups of females effectively. The quality and defensibility of resources affect mating systems, as does the defensibility of females. Population density of females also may be a critical determinant of the types of mating systems that develop. Size of groups likewise constrains the types of mating tactics that males can employ. Our aim was to use those relationships to create a broad conceptual model that predicts how various environmental and social factors interact to structure mating systems in ungulates. This model provides a useful framework for future tests of the roles of both ecological and social conditions in influencing the social systems of ungulates.     

Evolution of disassortative and assortative mating preferences based on imprinting

A two-locus haploid model of sexual selection is investigated to explore evolution of disassortative and assortative mating preferences based on imprinting. In this model, individuals imprint on a genetically transmitted trait during early ontogeny and choosy females later use those parental images as a criterion of mate choice. It is assumed that the presence or absence of the female preference is determined by a genetic locus. In order to incorporate such mechanisms as inbreeding depression and heterozygous advantage into our haploid framework, we assume that same-type matings are less fertile than different-type mating. The model suggests that: if all the females have a disassortative mating preference a viability-reducing trait may be maintained even without the fertility cost of same-type matings; a disassortative mating preference can be established even if it is initially rare, when there is a fertility cost of same-type matings. Further, an assortative mating preference is less likely to evolve than a disassortative mating preference. The model may be applicable to the evolution of MHC-disassortative mating preferences documented in house mice and humans.     

Female polyandry and size‐assortative mating in isolated local populations of the Japanese common toad Bufo japonicus

In anurans, female polyandry under male harassment is distributed across taxa because of external aquatic fertilization. According to the sexual selection theory, male–male competition for access to females is affected by the operational sex ratio (OSR) and population density. The Japanese common toad, Bufo japonicus, is widespread in mainland Japan, and like the European common toad, B. bufo, it engages in explosive breeding. In this study, we observed the breeding behaviour of B. japonicus in isolated local populations for over four years in two breeding ponds with different population sizes and densities: large‐low (L‐pond) and small‐high (S‐pond). We analysed the relative polyandry ratio in egg clutches laid by females and estimated the size‐assortative mating pattern to be an indicator of male–male competition in the two ponds. Both ponds tended to exhibit a size‐assortative mating pattern; however, the frequency of polyandry was different in the two ponds (L‐pond = 20% and S‐pond = 90%). Our results showed that polyandry could occur without multiple amplexus with a high population density, i.e. eggs were often fertilized by free‐swimming sperm in the small shallow pond. We propose that high female polyandry ratios without continuous male harassment are generated because of a male‐biased OSR and a high population density in the small pond. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 236–242.     

Social chromosome variants differentially affect queen determination and the survival of workers in the fire ant Solenopsis invicta

Intraspecific variation in social organization is common, yet the underlying causes are rarely known. An exception is the fire ant Solenopsis invicta in which the existence of two distinct forms of social colony organization is under the control of the two variants of a pair of social chromosomes, SB and Sb. Colonies containing exclusively SB/SB workers accept only one single queen and she must be SB/SB. By contrast, when colonies contain more than 10% of SB/Sb workers, they accept several queens but only SB/Sb queens. The variants of the social chromosome are associated with several additional important phenotypic differences, including the size, fecundity and dispersal strategies of queens, aggressiveness of workers, and sperm count in males. However, little is known about whether social chromosome variants affect fitness in other life stages. Here, we perform experiments to determine whether differential selection occurs during development and in adult workers. We find evidence that the Sb variant of the social chromosome increases the likelihood of female brood to develop into queens and that adult SB/Sb workers, the workers that cull SB/SB queens, are overrepresented in comparison to SB/SB workers. This demonstrates that supergenes such as the social chromosome can have complex effects on phenotypes at various stages of development.