Haplodiploid Sex Determination Research Articles

Hybridization in East African swarm-raiding army ants.

BackgroundHybridization can have complex effects on evolutionary dynamics in ants because of the combination of haplodiploid sex-determination and eusociality. While hybrid non-reproductive workers have been found in a range of species, examples of gene-flow via hybrid queens and males are rare. We studied hybridization in East African army ants (Dorylus subgenus Anomma) using morphology, mitochondrial DNA sequences, and nuclear microsatellites.ResultsWhile the mitochondrial phylogeny had a strong geographic signal, different species were not recovered as monophyletic. At our main study site at Kakamega Forest, a mitochondrial haplotype was shared between a "Dorylus molestus-like" and a "Dorylus wilverthi-like" form. This pattern is best explained by introgression following hybridization between D. molestus and D. wilverthi. Microsatellite data from workers showed that the two morphological forms correspond to two distinct genetic clusters, with a significant proportion of individuals being classified as hybrids.ConclusionsWe conclude that hybridization and gene-flow between the two army ant species D. molestus and D. wilverthi has occurred, and that mating between the two forms continues to regularly produce hybrid workers. Hybridization is particularly surprising in army ants because workers have control over which males are allowed to mate with a young virgin queen inside the colony.

Egg production and caste allocation in the clonally reproductive ant Vollenhovia emeryi

Sex ratio theories based on relatedness asymmetries among colony members have been tested in eusocial Hymenoptera. The haplodiploid sex determination system leads to differences in optimal sex allocation between queens and workers. Queens should ideally produce sexual eggs in accordance with relatedness asymmetries. One of the methods to test this hypothesis is to examine sex allocation in species where relatedness asymmetries are extremely different between female and males produced by the queens. We investigated sex allocation patterns in the polygynous ant Vollenhovia emeryi where both sexes are produced clonally so that the relatedness of the queens to their female and male offspring is 1.0 and 0, respectively. In this situation, queens invest most of their resources in female production. Furthermore, caste allocation patterns were observed in egg production. This study involved genotype analysis of colony members using genetic polymorphic markers and revealed clonal reproduction in the V. emeryi population. In this population, castes were identified in 1,060 eggs produced by 70 queens in 8 colonies. Queens invested more resources in female sexual eggs, though male eggs were also produced depending on resource availability. In addition, the proportion of female eggs negatively correlated with that of worker eggs, suggesting that this correlation is a tradeoff. However, male egg production did not affect the egg production of other castes. This observation indicates that male egg production is independent of that for other castes. This study is the first to document the real primary sex ratio and caste allocation in eusocial Hymenoptera. Key words: ant, clonal reproduction, egg, queen, sex ratio. [Behav Ecol]

Antibiotic treatment leads to the elimination of Wolbachia endosymbionts and sterility in the diplodiploid collembolan Folsomia candida

BackgroundWolbachia is an extremely widespread bacterial endosymbiont of arthropods and nematodes that causes a variety of reproductive peculiarities. Parthenogenesis is one such peculiarity but it has been hypothesised that this phenomenon may be functionally restricted to organisms that employ haplodiploid sex determination. Using two antibiotics, tetracycline and rifampicin, we attempted to eliminate Wolbachia from the diplodiploid host Folsomia candida, a species of springtail which is a widely used study organism.ResultsMolecular assays confirmed that elimination of Wolbachia was successfully achieved through continuous exposure of populations (over two generations and several weeks) to rifampicin administered as 2.7% dry weight of their yeast food source. The consequence of this elimination was total sterility of all individuals, despite the continuation of normal egg production.ConclusionMicrobial endosymbionts play an obligatory role in the reproduction of their diplodiploid host, most likely one in which the parthenogenetic process is facilitated by Wolbachia. A hitherto unknown level of host-parasite interdependence is thus recorded.

Phase-Unknown Linkage Mapping in Ants: Figure 1.

To create a genetic linkage map of an ant genome, the phase of a marker (i.e., which marker/allele came from the grandmother and which came from the grandfather of the individuals used for linkage mapping) must be known. However, field colonies contain only two generations: the queen(s) and their offspring. Normally, virgin queens disperse from their nest, mate with one or multiple males who die after mating, and start a new colony. A new reproductive brood (i.e., virgin queens and males) is usually produced after colony establishment, which can take from 6 mo to 3-5 yr. Hence, determining the phase of markers from field samples is impossible because the grandparents of a reproductive queen are no longer available for genetic analysis. Ants raised in the laboratory are likewise unsuitable for such analyses, because most ants cannot be bred regularly in the laboratory, and attempts to inseminate ant queens artificially have not been successful. However, three features facilitate "phase-unknown" linkage mapping for any ant (or other social hymenopteran) species, which is described here: (1) Mature colonies usually produce many reproductive offspring during a short period of time, which allows for the collection of a good-sized mapping population (>100 males) from a field colony; (2) Ants have a haplodiploid sex determination system (i.e., males are haploid and females diploid); (3) Queens produce males parthenogenetically. Thus, because they have no father, only those markers for which the queen is heterozygous are expected to segregate 1:1 in her male offspring.

Quantity matters: male sex pheromone signals mate quality in the parasitic wasp Nasonia vitripennis

Sexual selection theory asserts that females are well adapted to sense signals indicating the quality of potential mates. One crucial male quality parameter is functional fertility (i.e. the success of ejaculates in fertilizing eggs). The phenotype-linked fertility hypothesis (PLFH) predicts that functional fertility of males is reflected by phenotypic traits that influence female mate choice. Here, we show for Nasonia vitripennis, a parasitic wasp with haplodiploid sex determination and female-biased sex ratios, that females use olfactory cues to discriminate against sperm-limited males. We found sperm limitation in newly emerged and multiply mated males (seven or more previous matings) as indicated by a higher proportion of sons in the offspring fathered by these males. Sperm limitation correlated with clearly reduced pheromone titres. In behavioural bioassays, females oriented towards higher doses of the synthetic pheromone and were attracted more often to scent marks of males with a full sperm load than to those of sperm-limited males. Our data support the PLFH and suggest that N. vitripennis females are able to decrease the risk of getting constrained to produce suboptimal offspring sex ratios by orienting towards gradients of the male sex pheromone.

Comparative AFLP reveals paternal sex ratio chromosome specific DNA sequences in the parasitoid waspTrichogramma kaykai

The parasitoid wasp Trichogramma kaykai with a haplo-diploid sex determination has a B chromosome called the paternal sex ratio (PSR) chromosome that confers paternal genome loss during early embryogenesis, resulting in male offspring. So far, it is not well known whether the PSR chromosome has unique DNA sequence characteristics. By comparative AFLP fingerprinting of genomic DNA from wasps with and without the PSR chromosome, we isolated DNA from PSR-specific bands. Fourteen of such DNA fragments were analysed to confirm their PSR specificity. Seven were sequenced and two (PT-AFLP 1 and PT-AFLP1 3) were identified as parts of retrotransposon genes based on BLAST searches. Internal primers designed from a third AFLP fragment allowed PCR amplification of a PSR chromosome specific marker, which can be used to screen for the PSR trait in male wasps. Southern analysis revealed a dispersed repetitive nature of this third sequence in the T. kaykai genome, suggesting that it is part of a transposon. A fourth AFLP fragment (PT-AFLP 5) appears to be a large repetitive sequence on the PSR chromosome. This sequence is also found in the genome of both T. kaykai and the closely related species Trichogramma deion, but its distribution on the PSR chromosome strongly resembles that of T. deion rather than that of T. kaykai. Our results provide further insight into the repetitive nature of sequences comprising B chromosomes and their similarities with their host and closely related species.

Biology and Ecology of the Western Flower Thrips (Thysanoptera: Thripidae): The Making of a Pest

In the past 30 years, western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), has become one of the most important agricultural pests worldwide. Certain biological attributes of this insect predispose it to be a direct pest across a wide range of crops. In addition to the direct damage it can cause, this species is an efficient vector of Tomato spotted wilt virus and other Tospoviruses. This review addresses questions regarding the biological and ecological attributes of western flower thrips that have enabled it to become a significant pest and make it so difficult to manage. These important life history traits include western flower thrips polyphagy and a tendency to reside and feed in concealed areas of flowers and fruits. Consequently, large populations can develop and disperse into a wide range of crops. The larvae and adults feed in a similar manner and can share the same host plant resources. The relatively short generation time and haplodiploid sex determination also contribute to the pest status of this species. These life history traits interact in complex ways to make western flower thrips one of the most significant and difficult to manage pests in the world.

Genomic imprinting and kinship in the social Hymenoptera: What are the predictions?

The kinship theory of genomic imprinting predicts that conflicts of interest between parents can promote the evolution of opposed expression patterns of maternally and paternally derived alleles in the offspring. The social Hymenoptera (ants, some bees, and some wasps) are particularly suitable to test this theory, because a variety of social conflicts are predicted due to relatedness asymmetries between female and male nestmates that are a corollary of haplo-diploid sex determination. Here I argue that the kin-selection predictions for genomic imprinting in social Hymenoptera might in many cases be more complex than previously suggested, because the optimal strategy will have to take fitness effects in different castes and sexes into account.

Review. Lifelong commitment to the wrong partner: hybridization in ants.

The extraordinary lifelong partner commitment in social insects is expected to increase choosiness in both sexes and therefore to be associated with particularly low hybridization frequencies. Yet, more and more studies reveal that in many ant taxa hybrids are surprisingly common, with up to half of all female sexuals receiving sperm from allospecific males in extreme cases. In a few ant species, hybridization has led to the evolution of reproductively isolated new lineages with a bizarre system of genetic caste differentiation: colonies produce hybrid workers and pure-lineage female sexuals. This requires that colonies either contain multiple queens or that queens mate multiple times. In most other cases, hybridization appears to be an evolutionary dead end and fertile hybrid queens are rarely found. In such cases, haplodiploid sex determination appears to decrease the costs of mating with an allospecific male. As long as hybrid workers are viable, a cross-mated queen can partially rescue its fitness by producing males from unfertilized eggs. Mating with an allospecific partner may thus be an option for queens when conspecific mates are not available. The morphological similarity of most ant males, perhaps resulting from the lack of sexual conflict, may similarly contribute to the commoness of hybridization.

Invasion success of the bumblebee, Bombus terrestris, despite a drastic genetic bottleneck

In early 1992, the European bumblebee, Bombus terrestris, was first seen in Tasmania and currently has spread to most of the island. Here, we report on the genetic structure, using micro-satellites, of the invading population from samples collected in the years 1998-2000, a few years after the first sighting of the species in its new area. The data show that the Tasmanian population has a very low genetic diversity, with less than half of the allelic richness (Richness=2.89 alleles; H(exp)=0.591) and lower levels of heterozygosity as compared to populations in New Zealand (4.24 alleles; H(exp)=0.729) and Europe (5.08 alleles; H(exp)=0.826). In addition, the genetic data suggest that the invasion must have happened once, probably around late 1991, and was the result of very few, perhaps only two, individuals arriving in Tasmania. Furthermore, these founders came from the New Zealand population. Today, the population in the south of Tasmania seems to act as a source population from which individuals migrate into other parts of the state. A similar source-sink structure seems also the case for New Zealand. The data show that B. terrestris is a highly invasive species capable of establishing itself even after a dramatic genetic bottleneck. B. terrestris may be an invasive species due to the haplo-diploid sex determination system, which exposes recessive, deleterious mutations to selection. Offspring of such purged lines may then be able to tolerate high levels of inbreeding.

Clonal reproduction by males and females in the little fire ant

Sexual reproduction can lead to major conflicts between sexes and within genomes. Here we report an extreme case of such conflicts in the little fire ant Wasmannia auropunctata. We found that sterile workers are produced by normal sexual reproduction, whereas daughter queens are invariably clonally produced. Because males usually develop from unfertilized maternal eggs in ants and other haplodiploid species, they normally achieve direct fitness only through diploid female offspring. Hence, although the clonal production of queens increases the queen's relatedness to reproductive daughters, it potentially reduces male reproductive success to zero. In an apparent response to this conflict between sexes, genetic analyses reveal that males reproduce clonally, most likely by eliminating the maternal half of the genome in diploid eggs. As a result, all sons have nuclear genomes identical to those of their father. The obligate clonal production of males and queens from individuals of the same sex effectively results in a complete separation of the male and female gene pools. These findings show that the haplodiploid sex-determination system provides grounds for the evolution of extraordinary genetic systems and new types of sexual conflict.

OUTBREEDING DEPRESSION, BUT NO INBREEDING DEPRESSION IN HAPLODIPLOID AMBROSIA BEETLES WITH REGULAR SIBLING MATING

In sexual reproduction the genetic similarity or dissimilarity between mates strongly affects offspring fitness. When mating partners are too closely related, increased homozygosity generally causes inbreeding depression, whereas crossing between too distantly related individuals may disrupt local adaptations or coadaptations within the genome and result in outbreeding depression. The optimal degree of inbreeding or outbreeding depends on population structure. A long history of inbreeding is expected to reduce inbreeding depression due to purging of deleterious alleles, and to promote outbreeding depression because of increased genetic variation between lineages. Ambrosia beetles (Xyleborini) are bark beetles with haplodiploid sex determination, strong local mate competition due to regular sibling mating within the natal chamber, and heavily biased sex ratios. We experimentally mated females of Xylosandrus germanus to brothers and unrelated males and measured offspring fitness. Inbred matings did not produce offspring with reduced fitness in any of the examined life-history traits. In contrast, outcrossed offspring suffered from reduced hatching rates. Reduction in inbreeding depression is usually attributed to purging of deleterious alleles, and the absence of inbreeding depression in X. germanus may represent the highest degree of purging of all examined species so far. Outbreeding depression within the same population has previously only been reported from plants. The causes and consequences of our findings are discussed with respect to mating strategies, sex ratios, and speciation in this unusual system.

OUTBREEDING DEPRESSION, BUT NO INBREEDING DEPRESSION IN HAPLODIPLOID AMBROSIA BEETLES WITH REGULAR SIBLING MATING

In sexual reproduction the genetic similarity or dissimilarity between mates strongly affects offspring fitness. When mating partners are too closely related, increased homozygosity generally causes inbreeding depression, whereas crossing between too distantly related individuals may disrupt local adaptations or coadaptations within the genome and result in outbreeding depression. The optimal degree of inbreeding or outbreeding depends on population structure. A long history of inbreeding is expected to reduce inbreeding depression due to purging of deleterious alleles, and to promote outbreeding depression because of increased genetic variation between lineages. Ambrosia beetles (Xyleborini) are bark beetles with haplodiploid sex determination, strong local mate competition due to regular sibling mating within the natal chamber, and heavily biased sex ratios. We experimentally mated females of Xylosandrus germanus to brothers and unrelated males and measured offspring fitness. Inbred matings did not produce offspring with reduced fitness in any of the examined life-history traits. In contrast, outcrossed offspring suffered from reduced hatching rates. Reduction in inbreeding depression is usually attributed to purging of deleterious alleles, and the absence of inbreeding depression in X. germanus may represent the highest degree of purging of all examined species so far. Outbreeding depression within the same population has previously only been reported from plants. The causes and consequences of our findings are discussed with respect to mating strategies, sex ratios, and speciation in this unusual system.

Population structure, mating system, and sex-determining allele diversity of the parasitoid wasp Habrobracon hebetor.

Besides haplo-diploid sex determination, where females develop from fertilized diploid eggs and males from unfertilized haploid eggs, some Hymenoptera have a secondary system called complementary sex determination (CSD). This depends on genotypes of a 'sex locus' with numerous sex-determining alleles. Diploid heterozygotes develop as females, but diploid homozygotes become sterile or nonviable diploid males. Thus, when females share sex-determining alleles with their mates and produce low fitness diploid males, CSD creates a genetic load. The parasitoid wasp Habrobracon hebetor has CSD and displays mating behaviours that lessen CSD load, including mating at aggregations of males and inbreeding avoidance by females. To examine the influence of population structure and the mating system on CSD load, we conducted genetic analyses of an H. hebetor population in Wisconsin. Given the frequency of diploid males, we estimated that the population harboured 10-16 sex-determining alleles. Overall, marker allele frequencies did not differ between subpopulations, but frequencies changed dramatically between years. This reduced estimates of effective size of subpopulations to only N3 approximately 20-50, which probably reflected annual fluctuations of abundance of H. hebetor. We also determined that the mating system is effectively monogamous. Models relating sex-determining allele diversity and the mating system to female productivity showed that inbreeding avoidance always decreased CSD loads, but multiple mating only reduced loads in populations with fewer than five sex-determining alleles. Populations with N3 less than 100 should have fewer sex-determining alleles than we found, but high diversity could be maintained by a combination of frequency-dependent selection and gene flow between populations.

Mapping of paternal-sex-ratio deletion chromosomes localizes multiple regions involved in expression and transmission

The paternal-sex-ratio (PSR) chromosome in the parasitic wasp Nasonia vitripennis is a submetacentric supernumerary (B chromosome). Males transmit PSR, but after fertilization it causes the loss of the paternal autosomes. Paternal genome loss caused by PSR results in the conversion of a female (diploid) zygote into a male (haploid) under haplodiploid sex determination. In this study, site-specific markers were developed to assay deletion derivatives of PSR. Both polymerase chain reaction and Southern hybridization were used to detect the presence/absence of 16 single-site markers on a set of 20 functional and nine nonfunctional deletion chromosomes. Based on the pattern of marker loss on the deletion chromosomes, the basic organization of PSR was revealed. Two sets of markers were deleted independently, apparently representing the two arms of the submetacentric chromosome. The presence or absence of specific regions was examined in relation to phenotypic characteristics of the deletion chromosomes; ability to cause paternal genome loss, and stability in mitotic cell divisions. Rather than identifying a single region on PSR as being responsible for PSR function, the results suggest that the retention of one of two chromosomal regions is sufficient for causing paternal genome loss. Furthermore, a region was identified that is tightly correlated with mitotic stability, as measured from chromosomal transmission rates. Functional chromosomes with short-arm deletions had high (approximately 100%) transmission rates, whereas functional chromosomes with long-arm deletions had low (approximately 85%) transmission rates.

The birds and the wasps: a sex-ratio meta-analysis

Those who work on sex ratios of parasitoid wasps have long been lulled by the idea that, because of a haplo–diploid sex determination mechanism, these insects have a high degree of control over the sex of their progeny. Meanwhile, those working on birds and mammals have been subjected to the rather burdensome notion that heterogametic sex determination mechanisms severely constrain the production of biased sex ratios, and thus that these taxa are probably unable to achieve sex-ratio control. The latter view has been challenged recently by remarkable sex ratios in several higher vertebrate species, such as the Seychelles warbler Acrocephalus sechellensis; but does the constraint still hold in general? A new meta-analysis by West and Sheldon [ 1 West, S.A. and Sheldon, B.C. (2002) Constraints in the evolution of sex-ratio adjustment. Science 10.1126/science.1069043 Google Scholar ] of sex ratios in parasitoid wasps, birds and mammals concludes that it probably does not, and also that the sex ratios of wasps and birds are similarly influenced by environmental uncertainty.

COURTSHIP DISPLAYS OF INTROGRESSED, INTERSPECIFIC HYBRID NASONIA MALES: FURTHER INVESTIGATIONS INTO THE 'GRANDFATHER EFFECT'

Previously, we investigated courtship behaviour of bidirectional, interspecific hybrid males of two species of Nasonia (Beukeboom & van den Assem, 2001). Characteristics of the displays were intermediate between those of the parental species, but at the same time were biased towards the paternal side. Due to the haplodiploid sex determination system of the Hymenoptera, the nearest male parent of the haploid (hence, fatherless) Nasonia males are their grandfather. Therefore, we have called this bias the 'grandfather effect'. In the present paper, we investigate one of the possible causes of the 'grandfather effect': nucleocytoplasmic interaction. In interspecific hybrids, the paternally donated nuclear genes must operate in an 'alien' environment: the maternal (heterospecific) cytoplasm. Adverse effects may prevail in this situation, and result in a biased gene transmission (although to the maternal side). With introgression techniques and subsequent hybridisation of introgressed lines, we constructed male progeny in which paternally contributed nuclear genes are conspecific with the maternal cytoplasm. Courtship of these males provide a test of the interaction hypothesis. Because our results show a persistence of the 'grandfather effect', a simple nucleo-cytoplasmic interaction seems an unlikely explanation of the phenomenon.

Queen control of sex ratio in fire ants.

The haplodiploid sex-determination system of ants gives rise to conflict between queens and workers over colony sex ratios, and the female-biased allocation ratios seen in many species suggest that workers often prevail in this conflict. We exchanged queens between male- and female-specialist colonies of the fire ant Solenopsis invicta. These exchanges quickly reversed the sex-ratio biases of adopting colonies. The sex ratio of queen-laid eggs differed strongly between male- and female-specialist colonies. These findings suggest that queens can force workers to raise male sexuals by limiting the number of female brood and help to explain why sex investment ratios lie between the queen and worker equilibria in this and many other ant species.

Precise, highly female-biased sex ratios in a social spider.

It has been recognized for some time that the risk of producing maleless clutches should select for a lower than binomial variance in the sex ratio of organisms with female-biased sex ratios, small clutches and breeding groups containing the clutch of a single female. However, to date, precise sex ratios have only been reported for organisms with haplodiploid sex determination, a system which allows direct control of the sex of individual offspring. In contrast, under heterogametic sex determination chance is expected to play a crucial role in determining the sex composition of any one family, in particular when males are the heterogametic sex. Here, we present evidence of precise or underdispersed primary sex ratios in the Neotropical social spider Anelosimus domingo Levi. We show that this diplodiploid species with male heterogamety has not only beaten the odds of meiosis by producing mostly daughters, but has also attained relative precision in the proportion of sons and daughters produced in any one clutch. The latter finding suggests the existence of mechanisms that allow sorting of the two types of sperm in this spider species.

Reproductive alliances and posthumous fitness enhancement in male ants.

Ants provide excellent opportunities for studying the evolutionary aspects of reproductive conflict. Relatedness asymmetries owing to the haplodiploid sex determination of Hymenoptera create substantial fitness incentives for gaining control over sex allocation, often at the expense of the fitness interests of nest-mates. Under worker-controlled split sex ratios either the reproductive interests of the mother queen (when workers male bias the sex ratio) or the father (when workers female bias the sex ratio), but never that of both parents simultaneously, are fulfilled. When workers bias sex ratios according to the frequency of queen mating, males which co-sire a colony have a joint interest in manipulating their daughter workers into rearing a more female-biased sex ratio. Here we show that males of the ant Formica truncorum achieve such manipulation by partial sperm clumping, so that the cohort-specific relatedness asymmetry of the workers in colonies with multiple fathers is higher than the cumulative relatedness asymmetry across worker cohorts. This occurs because a single male fathers the majority of the offspring within a cohort. Colonies with higher average cohort-specific relatedness asymmetry produce more female-biased sex ratios. Posthumously expressed male genes are thus able to oppose the reproductive interests of the genes expressed in queens and the latter apparently lack mechanisms for enforcing full control over sperm mixing and sperm allocation.