With a few rare exceptions, the vast majority of animals reproduce sexually. Some species have, however, evolved alternative modes of reproduction by shifting from classical bisexuality to unorthodox reproductive systems, like parthenogenesis, gynogenesis, or hybridogenesis. Under hybridogenesis, both the maternal and paternal genomes are expressed in somatic tissues, whereas the germline is purely maternal. Recently, a form of hybridogenesis at the level of the society has been reported in some ants, where purebred females develop into reproductive queens and interlineage hybrids into sterile workers. Here, we report a unique case of social hybridogenesis in the desert ant Cataglyphis hispanica. Workers are produced exclusively from interbreeding between two distinct genetic lineages, whereas male and female sexuals are produced by asexual reproduction through parthenogenesis. As a consequence, all workers are pure hybridogens, and only maternal genes are perpetuated from one generation to the next. Thus, queens of C. hispanica use sexual reproduction for colony growth, whereas they reproduce asexually through parthenogenesis for germline production.

Hybridogenesis is a sexual reproductive system, whereby parents from different genetic origin hybridize. Both the maternal and paternal genomes are expressed in somatic tissues, but the paternal genome is systematically excluded from the germ line, which is therefore purely maternal. Recently, a unique case of hybridogenesis at a social level was reported in the desert ant Cataglyphis hispanica. All workers are sexually produced hybridogens, whereas sexual forms (new queens and males) are produced by queens through parthenogenesis. Thus, only maternal genes are perpetuated across generations. Here, we show that such an unusual reproductive strategy also evolved in two other species of Cataglyphis belonging to the same phylogenetic group, Cataglyphis velox and Cataglyphis mauritanica. In both species, queens mate exclusively with males originating from a different genetic lineage than their own to produce hybrid workers, while they use parthenogenesis to produce the male and female reproductive castes. In contrast to single-queen colonies of C. hispanica, colonies of C. velox and C. mauritanica are headed by several queens. Most queens within colonies share the same multilocus genotype and never transmit their mates' alleles to the reproductive castes. Social hybridogenesis in the desert ants has direct consequences on the genetic variability of populations and on caste determination. We also discuss the maintenance of this reproductive strategy within the genus Cataglyphis.

Recently, a unique case of hybridogenesis at a social level was reported in local populations of the desert ants Cataglyphis. Queens mate with males originating from a different genetic lineage than their own to produce hybrid workers, but they use parthenogenesis for the production of reproductive offspring (males and females). As a result, non-reproductive workers are all inter-lineage hybrids, whereas the sexual line is purely maternal. Here, we show that this unorthodox reproductive system occurs in all populations of the ant Cataglyphis hispanica. Remarkably, workers are hybrids of the same two genetic lineages along a 400 km transect crossing the whole distribution range of the species. These results indicate that social hybridogenesis in C. hispanica allows their maintenance over time and across a large geographical scale of two highly divergent genetic lineages, despite their constant hybridization. The widespread distribution of social hybridogenesis in C. hispanica supports that this reproductive strategy has been evolutionarily conserved over a long period.

French populations of the European corn borer consist of two sympatric and genetically differentiated host races. As such, they are well suited to study processes that could be involved in sympatric speciation, but the initial conditions of host-race divergence need to be elucidated. Gene genealogies can provide insight into the processes involved in speciation. We used DNA sequences of four nuclear genes to (1) document the genetic structure of the two French host races previously delineated with allozyme markers, (2) find genes directly or indirectly involved in reproductive isolation between host races, and (3) estimate the time since divergence of the two taxa and see whether this estimate is compatible with this divergence being the result of a host shift onto maize after its introduction into Europe ∼500 years ago. Gene genealogies revealed extensive shared polymorphism, but confirmed the previously observed genetic differentiation between the two host races. Significant departures from the predictions of neutral molecular evolution models were detected at three loci but were apparently unrelated to reproductive isolation between host races. Estimates of time since divergence between French host races varied from ∼75,000 to ∼150,000 years, suggesting that the two taxa diverged recently but probably long before the introduction of maize into Europe.

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Target pests may become resistant to Bacillus thuringiensis (Bt) toxins produced by trangenic maize (Zea mays L.). Untreated refuge areas are set aside to conserve high frequencies of susceptibility alleles: a delay in resistance evolution is expected if susceptible individuals from refuges mate randomly with resistant individuals from Bt fields. In principle, refuges can be toxin‐free maize or any other plant, provided it hosts sufficiently large pest populations mating randomly with populations from Bt‐maize fields. Our aim was to examine the suitability of several cultivated or weedy plants [pepper (Capsicum frutescens L.), sorghum (Sorghum spec.), sunflower (Helianthus annuus L.), cocklebur (Xanthium spec.), cantaloupe (Cucumis melo L.), and hop (Humulus lupulus L.)] as refuges for Ostrinia nubilalis (Hübner) (Lepidoptera: Crambidae) and Sesamia nonagrioides Lefebvre (Lepidoptera: Noctuidae), two major maize pests in southern Europe. Larvae of both species were collected on these plants. Their genetic population structure was examined at several allozyme loci. We found little or no evidence for an influence of geographic distance, but detected a significant host‐plant effect on the genetic differentiation for both species. Ostrinia nubilalis populations from sunflower, pepper, cocklebur, and sorghum appear to belong to the same genetic entity as populations collected on maize, but to differ from populations on hop. Accordingly, females from pepper and cocklebur produced exclusively the ‘Z’ type sexual pheromone, which, in France, characterizes populations developing on maize. Qualitatively, these plants (except hop) could thus serve as refuges for O. nubilalis; however, they may be of little use quantitatively as they were found much less infested than maize. Sesamia nonagrioides populations on maize and sorghum reached comparable densities, but a slight genetic differentiation was detected between both. The degree of assortative mating between populations feeding on both hosts must therefore be assessed before sorghum can be considered as a suitable refuge for this species.

In social organisms, the breeding system corresponds to the number of breeders in a group, their genetic relationships, and the distribution of reproduction among them. Recent, genetically based studies suggest an amazing array of breeding system and reproductive strategies in desert ants of the genus Cataglyphis. Using highly polymorphic DNA microsatellites, we performed a detailed analysis of the breeding system and population genetic structure of two Cataglyphis species belonging to the same phylogenetic group: C. niger and C. savignyi. Our results show that both species present very different breeding systems. C. savignyi colonies are headed by a single queen and populations are multicolonial. Remarkably, queens show one of the highest mating frequency reported in ants (Mp = 9.25). Workers can reproduce by both arrhenotokous and thelytokous parthenogenesis. By contrast, colonies of C. niger are headed by several, multiply mated queens (Mp = 5.17), and they are organized in supercolonial populations made of numerous interconnected nests. Workers lay arrhenotokous eggs only. These results illustrate the high variability in the socio-genetic organization that evolved in desert ants of the genus Cataglyphis.

Social insects exhibit remarkable variation in their colony breeding structures, both within and among species. Ecological factors are believed to be important in shaping reproductive traits of social insect colonies, yet there is little information linking specific environmental variables with differences in breeding structure. Subterranean termites (Rhinotermitidae) show exceptional variation in colony breeding structure, differing in the number of reproductives and degree of inbreeding; colonies can be simple families headed by a single pair of monogamous reproductives (king and queen) or they can be extended families headed by multiple inbreeding neotenic reproductives (wingless individuals). Using microsatellite markers, we characterized colony breeding structure and levels of inbreeding in populations over large parts of the range of the subterranean termites Reticulitermes flavipes in the USA and R. grassei in Europe. Combining these new data with previous results on populations of both species, we found that latitude had a strong effect on the proportion of extended-family colonies in R. flavipes and on levels of inbreeding in both species. We examined the effect of several environmental variables that vary latitudinally; while the degree of inbreeding was greatest in cool, moist habitats in both species, seasonality affected the species differently. Inbreeding in R. flavipes was most strongly associated with climatic variables (mean annual temperature and seasonality), whereas nonclimatic variables, including the availability of wood substrate and soil composition, were important predictors of inbreeding in R. grassei. These results are the first showing that termite breeding structure is shaped by local environmental factors and that species can vary in their responses to these factors.