Chromosomal variation among populations of a fungus-farming ant: implications for karyotype evolution and potential restriction to gene flow

Danon Clemes Cardoso,Jürgen Heinze,Mariana Neves Moura,Maykon Passos Cristiano

doi:10.1186/s12862-018-1247-5

Danon Clemes Cardoso, Jürgen Heinze + Show 2 more

Open Access

https://doi.org/10.1186/s12862-018-1247-5

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Abstract

BackgroundIntraspecific variation in chromosome structure may cause genetic incompatibilities and thus provides the first step in the formation of species. In ants, chromosome number varies tremendously from 2n = 2 to 2n = 120, and several studies have revealed considerable variation in karyotype within species. However, most previous studies were limited to the description of chromosome number and morphology, and more detailed karyomorphometric analyses may reveal additional, substantial variation. Here, we studied karyotype length, genome size, and phylogeography of five populations of the fungus-farming ant Trachymyrmex holmgreni in order to detect potential barriers to gene flow.ResultsChromosome number and morphology did not vary among the five populations, but karyotype length and genome size were significantly higher in the southernmost populations than in the northern populations of this ant. Individuals or colonies with different karyotype lengths were not observed. Karyotype length variation appears to result from variation in centromere length.ConclusionT. holmgreni shows considerable variation in karyotype length and might provide a second example of centromere drive in ants, similar to what has previously been observed in Solenopsis fire ants. Whether this variation leads to genetic incompatibilities between the different populations remains to be studied.

Highlights

Intraspecific variation in chromosome structure may cause genetic incompatibilities and provides the first step in the formation of species
Comparing each homologous chromosome across populations revealed that each chromosome individually contributed for variation in karyotype length in the CI and TO populations and seven pairs contributed to the variation in the Balneário Gaivota (BG) population (Fig. 2b, c): Chromosome 1 (GLM: Deviance(4,95) = 53.253, p < 0.001); Chromosome 2 (GLM: Deviance(4,95) = 36.995, p < 0.001); Chromosome 3 (GLM: Deviance(4,95) = 27.157, p < 0.001); Chromosome 4 (GLM: Deviance(4,95) = 20.856, p < 0.001); Chromosome 5 (GLM: Deviance(4,95) = 19.820, p < 0.001); Chromosome 6 (GLM: Deviance(4,95) = 18.241, p < 0.001), Chromosome 7 (GLM: Deviance(4,95) = 17.439, p < 0.001); Chromosome 8 (GLM: Deviance(4,95) = 16.236, p < 0.001); Chromosome 9 (GLM: Deviance(4,95) = 15.243, p < 0.001) and Chromosome 10 (GLM: Deviance(4,95) = 16.302, p < 0.001)
Mean genome size varied significantly between populations (GLM: Deviance(3,62) = 0.020538, p < 0.001) and the contrast analysis distinguished Cachoeira do Campo (CC) and Morro dos Conventos (MC) (0.31 ± 0.004 pg, 303.18 Mega base pairs (Mbp)) from BG (0.35 ± 0.003 pg, 342.3 Mbp), TO (0.35 ± 0.001 pg, 342.3 Mbp), and CI (0.35 ± 0.004 pg, 342.3 Mpb, Fig. 5). These results suggest that the genomes are 0.04 pg or 39.12 Mbp larger in the two populations with longer chromosomes (BG, TO and CI) than in the populations with shorter chromosomes (CC and MC)

Summary

Introduction

Intraspecific variation in chromosome structure may cause genetic incompatibilities and provides the first step in the formation of species. Chromosome number varies tremendously from 2n = 2 to 2n = 120, and several studies have revealed considerable variation in karyotype within species. Differences in chromosome number, form, and structure may result in genetic incompatibilities, which restrict gene flow among different lineages within a species [1,2,3,4], strengthen reproductive isolation among incipient species [5, 6], and prevent hybridization [7, 8]. Previous studies have shown that interspecific chromosomal variation differs among ant lineages [12,13,14]: clades that appear to have retained ancestral traits, such as the poneromorph subfamilies, often show large differences in chromosome number and even variation. Karyotypes differ between species due to Robertsonian rearrangements, inversions, and translocations ([12, 17], and in a number of genera chromosome mutations have been suggested to be involved in speciation (e.g., [12, 18])

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