Against the Odds: Hybrid Zones between Mangrove Killifish Species with Different Mating Systems

Abstract

Different mating systems are expected to affect the extent and direction of hybridization. Due to the different levels of sexual conflict, the weak inbreeder/strong outbreeder (WISO) hypothesis predicts that gametes from self-incompatible (SI) species should outcompete gametes from self-compatible (SC) ones. However, other factors such as timing of selfing and unilateral incompatibilities may also play a role on the direction of hybridization. In addition, differential mating opportunities provided by different mating systems are also expected to affect the direction of introgression in hybrid zones involving outcrossers and selfers. Here, we explored these hypotheses with a unique case of recent hybridization between two mangrove killifish species with different mating systems, Kryptolebias ocellatus (obligately outcrossing) and K. hermaphroditus (predominantly self-fertilizing) in two hybrid zones in southeast Brazil. Hybridization rates were relatively high (~20%), representing the first example of natural hybridization between species with different mating systems in vertebrates. All F1 individuals were sired by the selfing species. Backcrossing was small, but mostly asymmetrical with the SI parental species, suggesting pattern commonly observed in plant hybrid zones with different mating systems. Our findings shed light on how contrasting mating systems may affect the direction and extent of gene flow between sympatric species, ultimately affecting the evolution and maintenance of hybrid zones.

Genotyping-by-sequencing (GBS) as a tool for interspecies hybrid detection

“…Cases of hybridisation between two species with different mating systems were found in Kryptolebias ocellatus and K. hermaphroditus in two hybrid zones in Southeast Brazil (Berbel-Filho et al, 2021). The time of self-pollination and unilateral incompatibilities, in this case, was found to play a big role.…”

Additive and non-additive epigenetic signatures of natural hybridization between fish species with different mating systems

“…Here we only analysed the sympatric (i.e., coexisting) populations. Fish species were identified morphologically and confirmed by cytochrome oxidase subunit I (cox1) barcoding [ 41 ]. The nature of the hybrids analysed here was previously described in the first study of hybridization between these two species [ 41 ].…”

“…Fish species were identified morphologically and confirmed by cytochrome oxidase subunit I (cox1) barcoding [ 41 ]. The nature of the hybrids analysed here was previously described in the first study of hybridization between these two species [ 41 ]. Contrary to some theoretical expectations, all F1 hybrids we identified were sired by the rare males of the predominantly selfing species K. hermaphroditus , likely because their high selfing rates do not give much opportunity for outcrossing, either intra or interspecific.…”

“…A methylation-sensitive genotype-by-sequencing library (msGBS) was initially constructed using pectoral-fin samples of 55 hermaphrodite individuals (33 K . ocellatus and 22 K. hermaphroditus ) as detailed in [ 41 ] using a protocol modified from the genotype-by-sequencing protocol described in [ 42 , 43 ]. In brief, genomic DNA was digested using Eco RI and Hpa II and ligated to barcoded adapters.…”

“…To investigate cytosine methylation patterns, we selected 39 individuals with K. ocellatus (17) or K. hermaphroditus (22) with mtDNA haplotype from the two mangroves where they coexist (GUA and FUN; Supplementary Table S2). Among these, five F1 hybrids and two backcrossess were identified based on 16 microsatellites and SNP data as detailed in Berbel-Filho et al (2021) [ 41 ]. Differentially methylated cytosines (DMCs) were identified using the R package msgbsR [ 48 ].…”