High mating frequency and variation with lineage ratio in dependent-lineage harvester ants

Abstract

Explaining the evolution of multiple mating is a challenge because of the associated costs. For social insects, mating frequency may have fitness consequences due to effects on social interactions or genetic diversity within colonies. Here, we investigated the evolution of mating frequency in a social insect species with a unique genetic system that requires multiple mating. In certain populations of Pogonomyrmex harvester ants, there are two interbreeding yet genetically distinct mitochondrial lineages. Queens must mate with males of the opposite lineage to produce workers and with males of the same lineage to produce reproductive females. We expected queens of the dependent-lineage system to exhibit high mating frequencies relative to other social insects. Furthermore, we expected queens from populations of highly asymmetric lineage ratios to exhibit even higher mating frequencies, to adequately sample the population and successfully mate with males of the less common lineage. To test these predictions, we estimated the mating frequency of 16 P. barbatus queens, and compared these mating frequencies between two populations, one with relatively equal lineage ratio (60:40) and a second with a highly asymmetrical lineage ratio (96:4). Overall, observed mating frequency exceeded 10, which is high in comparison to other social insects, and our estimates of effective mating frequency were among the highest of Pogonomyrmex species. Mating frequency at the site with the asymmetrical lineage ratio was also significantly higher than the site with the more even ratio. Our results suggest that obligate multiple mating as well as lineage ratio contribute to the evolution of high mating frequency in dependent-lineage populations.

Inter-genomic sexual conflict drives antagonistic coevolution in harvester ants

“…We found no evidence of pre-mating discrimination between lineages in either the likelihood or latency of mating initiation. This is consistent with earlier studies demonstrating a significant correlation between the relative frequencies of the two lineages in the population at large and the relative mating success of males inferred from patriline distributions in adult colonies [26,27]. It is important to note, however, that males and/or females may still display preferences when both lineages are available for direct comparison; such simultaneous mate choice experiments could not be conducted here due to the time constraints caused by the limited duration of mating swarms and the difficulty of identifying lineage in the field.…”

“…In the absence of a pre-copulatory cue, males may instead benefit from maximizing mating frequency and thus limit the fitness consequences of any individual copulation [26]. For queens, the primary risk of a suboptimal mating distribution is failure to procure inter-lineage sperm required for worker production; the converse problem-failure to produce queen-destined progeny-is less costly because queens can recoup some fitness returns through parthenogenetically produced haploid male rspb.royalsocietypublishing.org Proc.…”

Sperm production characteristics vary with level of sperm competition inCataglyphisdesert ants

“…Van der Have, Boomsma & Menken ; Boomsma & Van Der Have ; Schlüns et al . ; Corley & Fjerdingstad ; Suni & Eldakar ). In total, we gathered information on sperm traits from a sample of 308 males across 15 species (see Table S1 in Supporting information).…”

“…This requirement is important since biogeographic variations in 1 000 000 2 000 000 3 000 000 4 000 000 5 000 000 population-specific paternity frequencies were previously documented in ants (e.g. Van der Have, Boomsma & Menken 1988;Boomsma & Van Der Have 1998;Schl€ uns et al 2009;Corley & Fjerdingstad 2011;Suni & Eldakar 2011). In total, we gathered information on sperm traits from a sample of 308 males across 15 species (see Table S1 in Supporting information).…”

Discrimination of conspecifics from heterospecifics in a hybrid zone: Behavioral and chemical cues in ants

“…Consequently, accurate identification of the potential mates' species before copulation could be undermined. In the absence of precopulatory cues, reproductives may benefit from maximizing mating frequency as breeding with a wrong partner could have a more negligible consequence on fitness, e.g., if females mate with multiple males (El-Shehaby et al, 2011;Suni these species (Cordonnier et al, 2020c) could help to solve this question in the future, for instance in studying the occurrence of mixed mating (i.e., queens of a given species mated with both heterospecific and conspecific male(s)). Conversely, the findings could be similar in reproductive than in workers, suggesting that reproductive could discriminate heterospecifics, but mate with both conspecifics and heterospecifics.…”