Inversions and genomic differentiation after secondary contact: When drift contributes to maintenance, not loss, of differentiation

Due to their effects on reducing recombination, chromosomal inversions may play an important role in speciation by establishing and/or maintaining linked blocks of genes causing reproductive isolation (RI) between populations. This view fits empirical data indicating that inversions typically harbor loci involved in RI. However, previous computer simulations of infinite populations with two to four loci involved in RI implied that, even with gene flux as low as 10–8 per gamete, per generation between alternative arrangements, inversions may not have large, qualitative advantages over collinear regions in maintaining population differentiation after secondary contact. Here, we report that finite population sizes can help counteract the homogenizing consequences of gene flux, especially when several fitness-related loci reside within the inversion. In these cases, the persistence time of differentiation after secondary contact can be similar to when gene flux is absent and notably longer than the persistence time without inversions. Thus, despite gene flux, population differentiation may be maintained for up to 100,000 generations, during which time new incompatibilities and/or local adaptations might accumulate and facilitate progress toward speciation. How often these conditions are met in nature remains to be determined.This study was supported by the European Regional Development Fund (FCOMP-01-0124-FEDER-014272), FCT – Foundation for Science and Technology (PTDC/BIA-EVF/113805/2009), Ministerio de Ciencia e Innovación, Spain (PGC2018-101927-B-I00, MINECO/FEDER, UE), by the Spanish National Institute of Bioinformatics (PT17/0009/0020), and by “Unidad de Excelencia María de Maeztu,” funded by the MINECO (ref: MDM-2014-0370). MR was funded by the Hasselblad Foundation (Grant for Female Scientists), European Research Council and the Swedish Research Councils VR and Formas (Linnaeus grant to the Centre for Marine Evolutionary Biology), and by an additional grant from Formas (to MR; grant number 2019-00882). JLF was funded by support from the National Science Foundation and United States Department of Agriculture NIFA program. RF was funded by FCT (SFRH/BPD/89313/2012) and by the European Union's Horizon 2020 research and innovation program, under the Marie Sklodowska-Curie grant agreement number 706376; and is currently funded by FEDER through the Operational Competitiveness Factors Program COMPETE and by National Funds through the FCT project “Hybrabbid” (PTDC/BIA-EVL/30628/2017 and POCI-01-0145-FEDER-030628). The simulations were performed on resources at Chalmers Centre for Computational Science and Engineering (C3SE), and at National Supercomputer Centre at Linköping University (NSC) provided by the Swedish National Infrastructure for Computing (SNIC), partially funded by the Swedish Research Council through grant agreement no. 2018–05973.Peer reviewe