Evolution of hybridogenetic lineages in Cataglyphis ants

Abstract

In most social Hymenoptera, a diploid egg develops into either a queen or a worker depending on environmental conditions. Hybridogenetic Cataglyphis ants display a bizarre genetic system, where queen‐worker caste determination is primarily determined by genetic factors. In hybridogenetic populations, all workers are F1 hybrids of two distinct lineages, whereas new queens are nearly always pure‐lineage individuals produced by clonal reproduction. The distribution and evolutionary history of these hybridogenetic populations have not yet been thoroughly analysed. Here, we studied the phylogeographic distribution of hybridogenetic populations in two closely related Spanish species: Cataglyphis humeya and Cataglyphis velox. Hybridogenesis has been previously documented in a locality of C. velox, but whether this system occurs elsewhere within the range of the two species was yet unknown. Queens and workers from 66 localities sampled across the range of the species were genotyped at 18 microsatellite markers to determine whether queens were produced by parthenogenesis and whether workers were hybrids of divergent lineages. Populations with F1 hybrid workers were identified by combining genetic, geographical and mating assortments data. In most populations of C. velox, workers were found to be hybrids of two divergent lineages. Workers were however produced via random mating in two marginal populations of C. velox, and in all populations studied of its sister species C. humeya. High‐throughput sequencing data were obtained to confirm inferences based on microsatellites and to characterize relationships between populations. Our results revealed a complicated history of reticulate evolution that may account for the origin of hybridogenetic lineages in Cataglyphis.

Repeated evolution of queen parthenogenesis and social hybridogenesis in Cataglyphis desert ants

“…Experimental laboratory observations revealed that only a very small proportion of worker‐laid haploid eggs and none of diploid eggs reach adulthood (Leniaud et al, ; Eyer et al, ; A. Kuhn and H. Darras, personal observation). In line with this, across all hybridogenetic Cataglyphis species studied so far, the hundreds of reproductive individuals collected from the field were of pure breeding lineages – no hybrid males or queens (except one; Darras et al, ) have been found, making very unlikely that worker‐laid eggs (if any) achieve their development into viable and fertile hybrid sexuals. Altogether, these results suggest that obligate crossing may have lessened worker fertility, thereby reducing queen‐worker conflict over male and female parentage within colonies.…”

“…In contrast, in nonhybridogenetic species or populations, workers are produced by sexual reproduction between partners belonging to the same gene pool (random mating). To determine whether or not workers resulted from hybrid matings, we analysed genetic variability among reproductive individuals and determined whether mating patterns were disassortative or random using the genotype webs approach (Darras et al, ). For each species, a Principal Coordinate Analysis (PCoA) based on the genotypes of the reproductives (the mother queens and their inferred male mates) was performed with genalex version 6.502 (Peakall & Smouse, , ).…”

“…DNA was extracted from the adult ants and the sperm samples using the Chelex 100 method (Kuhn et al, 2017;Walsh, Metzger, & Higuchi, 1991). A total of 22 microsatellite markers were used: Cc11, Cc54, Cc76, Cc89, Cc93, Cc99, Ch01, Ch05, Ch06, Ch08, Ch11, Ch12, Ch22, Ch23, Ch25 (Darras, Leniaud, et al, 2014;Pearcy, Clémencet, et al, 2004), Ch10, Ch19 (Darras et al, 2019), Cm01, Cm03, Cm07, Cm11, and Cn03 (this study; Table S2). For each species, the adult ants and the sperm samples were genotyped at 7-10 microsatellite loci (Table S3).…”

“…As a result, nonreproductive workers are all interlineage hybrids, while queens and males are all pure lineage individuals. Deviation from this caste‐genotype association is extremely rare in natural colonies of hybridogenetic species of Cataglyphis (Darras Kuhn, & Aron, , ; Eyer et al, ; Kuhn, Darras, & Aron, ).…”

“…The conditional use of sex appears to have a limited phylogenetic distribution. It has been documented in all the species of the altisquamis group that have been surveyed to date ( Cataglyphis hispanica , C. humeya , C. mauritanica , and C. velox ; Darras, Kuhn, & Aron, ; Eyer et al, ; Leniaud et al, ), as well as in one species of the cursor group ( C. piliscapa , previously known as C. cursor var. piliscapa ; Pearcy, Aron, et al, ; Table ).…”