As a PhD student studying the effects of genetic diversity overall and immunogenetic diversity specifically on survival and reproductive success in an endangered primate in captive and wild populations, I thought a lot about the potential effects of inbreeding and outbreeding depression. I read literally 100s of papers on the topic. Inbreeding depression describes the negative fitness effects that can occur in small populations when relatives breed with each other for multiple generations, thus genetic diversity is lost through genetic drift and negative alleles are expressed. Outbreeding depression, by contrast, is the negative consequence of breeding two genetically distinct populations leading to a loss of local adaptation.
Concerns about outbreeding depression are one of the major theoretical limitations to re-introductions and attempts at ‘genetic rescues’ when small populations and/or endangered species might be suffering from inbreeding depression. For the most part, however, evidence of outbreeding depression has mostly been limited to plants and captive or laboratory studies. Earlier this year, however, Dr. Sarah Fitzpatrick and her co-authors documented an extremely cool example of genetic rescue in populations of wild Trinidadian guppies, contradicting the hypothesis about the potential for maladaptive gene flow in population introductions (Fitzpatrick et al. 2020).
After repeatedly sampling two isolated guppy ‘recipient’ populations (Figure 1A, dark blue circles, N < 100 individuals per population) in the Caigual and Taylor rivers in Trinidad, the authors introduced populations of guppies upstream (dashed red circles) of these recipient populations, in previously guppy-free areas. These trans-located guppies, from downstream populations (solid red circles), occasionally (or frequently!) migrated downstream into the recipient populations located either ~5m or ~700m from the introduction location. For ~8-10 guppy generations after the trans-location, the recipient populations have been monitored with mark-recapture to assess population size as well as individual overall genetic diversity, hybrid ancestry, lifespan, and reproductive success. Following the onset of immigration and subsequent gene flow, both recipient populations experienced nearly a 10-fold increase in population size, from less than 100 individuals to an estimated 1,000 individuals each (Figure 1B). Based on the hybrid index, which ranges from 0 to 1 based on the amount of native or immigrant ancestry of an individual respectively, of the generations, it’s clear that 10 generations after the first wave of immigration, the population consists almost entirely of admixed individuals (Figure 1C).
Contradicting the predictions of outbreeding depression, individuals with intermediate to high (0.5-0.75) hybrid indices had the highest longevity and reproductive success in both locations and across sexes (Figure 2). Interestingly, although hybrids and pure immigrants had similar levels of genetic heterozygosity, hybrids had higher fitness, suggesting that increased genomic diversity alone does not explain the increased fitness and pointing towards a potential maintenance of locally adapted alleles.
Pre-introduction, 95% and 96% of >12,000 genotyped SNPs were monomorphic in the Caigual and Taylor populations respectively and average nucleotide diversity was 0.01 in both populations (Figure 4b). 8-10 generations later, only 22 and 24% of SNPs are monomorphic and nucleotide diversity has increased to 0.21 and 0.22. Genome-wide average Fst between source and recipient populations also decreased from 0.29-0.31 to 0.01.
To determine if gene flow swamped locally adaptive variants, the authors identified 146 loci with allele frequencies in the pre-immigrant recipient populations that might indicate candidacy for locally adapted alleles. Post-immigration, although overall genome homogenization increased between immigrant and recipient populations, the authors found evidence for selective maintenance of some of the candidate alleles in the recipient populations in the form of an excess of pre-immigrant ancestry at these loci (Fig 4). Unfortunately, none of these candidate loci matched previously identified loci under selection nor were any gene ontology terms enriched, but they provide interesting potential targets for future investigation.
This study documents the phenomenon of genetic rescue in two multi-generational wild populations, showing that contrary to expectations, gene flow does not necessarily swam local adaptation, and actually can significantly increase fitness in the form of longevity and reproductive success, subsequently substantially increasing population size. Further, at laest some locally adapted loci appear to have been maintained in both Caigual and Taylor, despite a 10-fold difference in the number of immigrants to each population, suggesting a range of gene flow rates might still allow the maintenance of local adaptation, with extremely important and interesting implications for future conservation-based introduction efforts.
Fitzpatrick, S.W., G.S. Bradburd, C.K. Kremer, P.E. Salerno, L.M. Angeloni, W.C. Funk (2020) Genomic and fitness consequences of genetic rescue in wild populations. Current Biology 30: 517-522.e5.