Speciation and hybridization in invasive fire ants

Abstract

Background A major focus of evolutionary biology is the formation of reproductive barriers leading to divergence and ultimately, speciation. Often, it is not clear whether the separation of populations is complete or if there still is ongoing gene flow in the form of rare cases of admixture, known as isolation with migration. Here, we studied the speciation of two fire ant species, Solenopsis invicta and Solenopsis richteri , both native to South America, both inadvertently introduced to North America in the early twentieth century. While the two species are known to admix in the introduced range, in the native range no hybrids were found. Results We conducted a population genomic survey of native and introduced populations of the two species using reduced representation genomic sequencing of 337 samples. Using maximum likelihood analysis over native range samples, we found no evidence of any gene flow between the species since they diverged. We estimated their time of divergence to 190,000 (100,000–350,000) generations ago. Modelling the demographic history of native and introduced S. invicta populations, we evaluated their divergence times and historic and contemporary population sizes, including the original founder population in North America, which was estimated at 26 (10–93) unrelated singly-mated queens. Conclusions We provide evidence for complete genetic isolation maintained between two invasive species in their natïve range, based, for the first time, on large scale genomic data analysis. The results lay the foundations for further studies into different stages in the formation of genetic barriers in dynamic, invasive populations. Electronic supplementary material The online version of this article (10.1186/s12862-019-1437-9) contains supplementary material, which is available to authorized users.

The social supergene dates back to the speciation time of two Solenopsis fire ant species

“…This analysis was based on Restriction site Associated DNA sequencing (RAD-seq) data of S. invicta and S. richteri populations samples from Argentina, which we described in Cohen and Privman 25 . We used sequences of four homozygote SB / SB and four homozygote Sb / Sb richteri workers from the population of Buenos Aires, Argentina.…”

“…We filtered out loci that had less than 6 reads in more than one individual. Additionally, we used a SNPs catalogue that was previously created from the RAD-sequencing of the 4 SB/SB and 4 Sb/Sb samples of S. richteri from the native range 25 . We kept loci that had at least 6 reads in all individuals (as we only have 4 individuals per social haplotype).…”

“…Such an event may have been driven by adaptive introgression as suggested for other loci of high fitness effect 21 – 24 . In a previous study, we used a coalescent-based analysis to date the separation of two social polymorphic species, S. invicta and S. richteri , to 1.1 (0.6–2.1) million years ago, assuming generation time of 6 years 25 . Additionally, we found no evidence of historic admixture between them, despite the large scale genomic data that was analyzed.…”

“…For comparison, in the same study the Attini lineage, that includes the two leafcutter ants, was found to have diverged from the Solenopsis lineage approximately 80 MYA. Additionally, reduced genomic sequencing of a large number of S. richteri samples is now available 25 , allowing the studying of the social chromosome outside of S. invicta .…”

From Pavement to Population Genomics: Characterizing a Long-Established Non-native Ant in North America Through Citizen Science and ddRADseq

“…Population genomic approaches, in particular, restriction siteassociated DNA sequencing (RADseq) (Miller et al, 2007;Baird et al, 2008;Peterson et al, 2012), offer a cost-effective solution for surveying genome-wide single nucleotide polymorphism (SNPs) in species without a sequenced genome. These techniques have proven useful to understanding species' invasion histories (Dupuis et al, 2018;Leydet et al, 2018;Bors et al, 2019;Cohen and Privman, 2019) and as a non-destructive method for identification and monitoring (reviewed in Taylor and Gemmell, 2016). More generally, emergence of RAD-based techniques have led to wide adoption of these methods in ecological and evolutionary studies of insects (Bagley et al, 2017;Storer et al, 2017;Lower et al, 2018;Zhang et al, 2018;De Jesús-Bonilla et al, 2019), including ants (Moreau and Wray, 2017;Boyle et al, 2018;Avril et al, 2019;Smith et al, 2019), which rank among the most damaging and difficult to control invasive species (Rabitsch, 2011).…”