Multigenerational hybridisation results in heterosis and facilitates adaptive introgression, with no evidence of outbreeding depression in a pair of marine gastropods

Cummins, Deanne 1 ; Johnson, Michael S.1 ; Tomkins, Joseph L.1 ; Kennington, W. Jason1

Published Dec 02, 2024 on Dryad. https://doi.org/10.5061/dryad.zw3r228j3

Data files

Dec 02, 2024 version files 89.80 MB

Abstract

Anthropogenic environmental changes continue to threaten species globally. For example, translocation of species has caused unintentional hybridisation, which has contributed to species declines. On the other hand, hybridisation can be used to increase the evolutionary potential of species vulnerable to rapid environmental change, although the benefits of mixing genetically divergent lineages do not come without risks to individual fitness and the long-term viability of populations. Here, we use a combination of genome-wide Single Nucleotide Polymorphism (SNP) markers, mitochondrial DNA sequencing and measurements of growth rate to determine the genetic consequences of hybridisation between two congeneric marine gastropods across 27 years (~ 18 generations). Multigeneration hybridisation resulted from the introduction of the intertidal periwinkle Bembicium vittatum (a direct developer) into the native range of its congener Bembicium auratum (a species with planktotrophic larval dispersal). Despite significant genetic divergence between the species, we found no direct evidence of outbreeding depression in the admixed population. Instead, we found evidence for heterosis, which dissipated over time. After an initial lag, the frequency of introduced B. vittatum alleles declined dramatically in the hybrid population. However, a few B. vittatum alleles (3.18%) increased significantly in frequency against the overall trend, providing evidence of adaptive introgression. In the context of hybridisation as a conservation management tool, our results provide some evidence of the potential benefits that can be gained, and suggest that the costs due to outbreeding depression can be small.

README: Multigenerational hybridisation results in heterosis and facilitates adaptive introgression, with no evidence of outbreeding depression in a pair of marine gastropods

Description of the data and file structure

"SNPdata_DBemb21-6115_2_SNP_mapping_2.csv" contains raw SNP genotype data generated by Diversity Arrays Technology for each individual used in the study. Each allele is scored in binary fashion ("1"=Presence and "0"=Absence) and heterozygotes are scored as 1/1 (presence for both alleles/both rows). This SNP dataset matches the one published alongside our previous study (https://doi.org/10.5061/dryad.g4f4qrfz4).

Locus metatdata is also contained in this file (generated by DArT) including allele identification (AlleleID), the seaquence of each allele (AlleleSequence), average count of the reference (AvgCountRef) and SNP allele (AvgCountSnp), average polymorphism content of each locus (AvgPIC), locus call rate (CallRate), a unique identifier for the sequence that each SNP occurs in (CloneID), the proportion of samples scored as heterozygotes for each locus (FreqHets), the proportion of samples scored as homozygous for the reference allele (FreqHomRef) and SNP allele (FreqHomSnp), the polymorphism information content for the reference allele (PICRef) and the SNP allele (PICSnp), the proportion of technical replicates where the marker score is consistent (RepAvg), the position within the sequence tag where the SNP occurs (SnpPosition), and a trimmed version of the full sequence, but with adapters removed in shorter marker tags (TrimmedSequence).

"individual_metadata_dryad.xlsx" contains individual metadata, including individual identification, population code, year collected, latitude, longitude, species classification and haplotype information based on 12S sequences for individuals collected in Fremantle and the B. vittatum and B. auratum source populations. The haplotype columns (Species haplotype, Haplotype and GenBank Accession) contain and N/A if haplotype information was not collected for that individual. The metadata also includes standardised growth rate measurements for individuals collected from the Fremantle population in 2007 and 2020. The growth rate of other individuals was not measured, hence all other individuals have N/A in the growth rate column. Additionally, for individuals collected from Fremantle in 2007 and 2020 we have included the structure membership coefficient and observed heterozygosity, calculated using all filtered SNPs and diagnostic loci. Again, all other individuals have N/A for these metrics because they were not included in that particular analysis.

"All_Fremantle_analyses.R" contains the code used to conduct all analyses pertaining to hybridisation and data filtering for this study, "Outlier_loci_analysis.R" contains the code used for outlier analyses using the B. vittatum source populations and "Plots.R" contains the code used to create all figures except the boxplots in Figure 2 of the manuscript. The code for those is in the analysis file.