Male‐biased dispersal in a fungus‐gardening ant symbiosis

Abstract

For nearly all organisms, dispersal is a fundamental life‐history trait that can shape their ecology and evolution. Variation in dispersal capabilities within a species exists and can influence population genetic structure and ecological interactions. In fungus‐gardening (attine) ants, co‐dispersal of ants and mutualistic fungi is crucial to the success of this obligate symbiosis. Female‐biased dispersal (and gene flow) may be favored in attines because virgin queens carry the responsibility of dispersing the fungi, but a paucity of research has made this conclusion difficult. Here, we investigate dispersal of the fungus‐gardening ant Trachymyrmex septentrionalis using a combination of maternally (mitochondrial DNA) and biparentally inherited (microsatellites) markers. We found three distinct, spatially isolated mitochondrial DNA haplotypes; two were found in the Florida panhandle and the other in the Florida peninsula. In contrast, biparental markers illustrated significant gene flow across this region and minimal spatial structure. The differential patterns uncovered from mitochondrial DNA and microsatellite markers suggest that most long‐distance ant dispersal is male‐biased and that females (and concomitantly the fungus) have more limited dispersal capabilities. Consequently, the limited female dispersal is likely an important bottleneck for the fungal symbiont. This bottleneck could slow fungal genetic diversification, which has significant implications for both ant hosts and fungal symbionts regarding population genetics, species distributions, adaptive responses to environmental change, and coevolutionary patterns.

Cophylogenetic analyses of Trachymyrmex ant‐fungal specificity: “One to one with some exceptions”

“…However, we did not include any of these mtDNA sequences in the analyses because the chromatograms of T. arizonensis appeared to lack variation and contained abnormal peaks. In contrast, the chromatograms of T. pomonae revealed readable sequences similar to the closely related T. septentrionalis (Matthews et al, 2021;Seal et al, 2015). Although "numts" (mitochondrial-like nuclear sequences) have been reported in closely related ants (Beckenbach, 2009;Cristiano et al, 2014;Martins et al, 2007), we did not explore this possibility in T. arizonensis; however, the lack of variation and irregular peaks suggested issues with this region of the mitochondrial (Freeland, 2006).…”

“…Moreover, most Clade B4 fungi grown by these four ant species had nearly identical ITS sequences with those of fungi grown by distantly related ants in Brazil (Luiso et al, 2020). Although much about the dispersal abilities of the ants and fungi remains to be discovered (Matthews et al, 2021;Smith et al, 2019), it is unlikely that the same clone of fungi is cultivated by different host species in Arizona, Florida, and Brazil based on geographical distance alone. Instead, the genetic similarity and lack of geographic variation is probably a consequence of the limited power or evolutionary bias in the genetic markers used.…”

Trachymyrmex septentrionalis ant microbiome assembly is unique to individual colonies and castes

“…The 20 different microbiomes possessed by these castes could therefore reflect their need to reproduce, which the workers do not experience. Female alates possess large amounts of lipids, proteins, and carbohydrates to provide energy when they start their colonies [63], and male alates must travel further than female alates to mate [64]. The different microbiome composition possessed by male and female alates (Fig.…”

“…The different microbiome composition possessed by male and female alates (Fig. 3C) could therefore reflect the differing energy and nutrient requirements of their different reproductive behaviors [63,64].…”

“…The different microbiome composition possessed by male and female alates (Fig. 3C) could therefore reflect the differing energy and nutrient requirements of their different reproductive behaviors (64, 65). Although we show that T. septentrionalis microbiomes differ between castes, how vertical versus environmental transmission contributes to these differences remains unknown.…”