Consequences of Hybridization in Mammals: A Systematic Review

Hybridization, defined as breeding between two distinct taxonomic units, can have an important effect on the evolutionary patterns in cross-breeding taxa. Although interspecific hybridization has frequently been considered as a maladaptive process, which threatens species genetic integrity and survival via genetic swamping and outbreeding depression, in some cases hybridization can introduce novel adaptive variation and increase fitness. Most studies to date focused on documenting hybridization events and analyzing their causes, while relatively little is known about the consequences of hybridization and its impact on the parental species. To address this knowledge gap, we conducted a systematic review of studies on hybridization in mammals published in 2010–2021, and identified 115 relevant studies. Of 13 categories of hybridization consequences described in these studies, the most common negative consequence (21% of studies) was genetic swamping and the most common positive consequence (8%) was the gain of novel adaptive variation. The total frequency of negative consequences (49%) was higher than positive (13%) and neutral (38%) consequences. These frequencies are biased by the detection possibilities of microsatellite loci, the most common genetic markers used in the papers assessed. As negative outcomes are typically easier to demonstrate than positive ones (e.g., extinction vs hybrid speciation), they may be over-represented in publications. Transition towards genomic studies involving both neutral and adaptive variation will provide a better insight into the real impacts of hybridization.

Selection for biparental inheritance of mitochondria under hybridization and mitonuclear fitness interactions

Uniparental inheritance (UPI) of mitochondria predominates over biparental inheritance (BPI) in most eukaryotes. However, examples of BPI of mitochondria, or paternal leakage, are becoming increasingly prevalent. Most reported cases of BPI occur in hybrids of distantly related sub-populations. It is thought that BPI in these cases is maladaptive; caused by a failure of female or zygotic autophagy machinery to recognize divergent male-mitochondrial DNA ‘tags’. Yet recent theory has put forward examples in which BPI can evolve under adaptive selection, and empirical studies across numerous metazoan taxa have demonstrated outbreeding depression in hybrids attributable to disruption of population-specific mitochondrial and nuclear genotypes (mitonuclear mismatch). Based on these developments, we hypothesize that BPI may be favoured by selection in hybridizing populations when fitness is shaped by mitonuclear interactions. We test this idea using a deterministic, simulation-based population genetic model and demonstrate that BPI is favoured over strict UPI under moderate levels of gene flow typical of hybridizing populations. Our model suggests that BPI may be stable, rather than a transient phenomenon, in hybridizing populations.

Fitness consequences of targeted gene flow to counter impacts of drying climates on terrestrial-breeding frogs

Targeted gene flow (TGF) could bolster the adaptive potential of isolated populations threatened by climate change, but could also lead to outbreeding depression. Here, we explore these possibilities by creating mixed- and within-population crosses in a terrestrial-breeding frog species threatened by a drying climate. We reared embryos of the crawling frog (Pseudophryne guentheri) on wet and dry soils and quantified fitness-related traits upon hatching. TGF produced mixed outcomes in hybrids, which depended on crossing direction (origin of gametes from each sex). North-south crosses led to low embryonic survival if eggs were of a southern origin, and high malformation rates when eggs were from a northern population. Conversely, east-west crosses led to one instance of hybrid vigour, evident by increased fitness and desiccation tolerance of hybrid offspring relative to offspring produced from within-population crosses. These contrasting results highlight the need to experimentally evaluate the outcomes of TGF for focal species across generations prior to implementing management actions.

The genetics of assisted gene flow: immediate costs and long-term benefits

ABSTRACTPlant and animal populations are facing several novel risks such as human-mediated habitat fragmentation and climate change that threaten their long-term productivity and persistence. With the genetic health of many populations deteriorating due to climate change outpacing physiological adaptation, human interventions in the form of assisted gene flow (AGF) may provide genetic variation to adapt populations to predicted climate change scenarios and result in more robust and productive populations. We ran genetic simulations to mimic a variety of AGF scenarios and measured their outcomes on population-level fitness to answer the question: in which circumstances is it worthwhile to perform AGF? Based on the parameters we explored, AGF may be harmful in certain situations over the short term (e.g., the first ∼10-20 generations), due to outbreeding depression and introducing deleterious genetic variation. Moreover, under many parameter sets, the benefits of AGF were relatively weak or took many generations to accrue. In general, when the adaptive trait is controlled by many loci of small effect, the benefits of assisted gene flow take much longer to realize–potentially too long for most climate-related management decisions. We also show that when translocation effort is divided across several generations and outbreeding depression is strong, the recipient population experiences a smaller decrease in fitness as compared to moving all individuals in a single effort. Importantly, in most cases, we show that the genomic integrity of the recipient population remains relatively intact following AGF; the amount of genetic material from the donor population typically ends up constituting no more of the recipient population’s genome than the fraction introduced. Our results will be useful for conservation practitioners and silviculturists, for instance, aiming to intervene and adaptively manage so that populations maintain a robust genetic health and maintain productivity into the future given anthropogenic climate change.

Outbreeding depression as a selective force on mixed mating in the mangrove rivulus fish,Kryptolebias marmoratus

Mixed mating, a reproduction strategy utilized by many plants and invertebrates, optimizes the cost to benefit ratio of a labile mating system. One type of mixed mating includes outcrossing with conspecifics and self-fertilizing one’s own eggs. The mangrove rivulus fish (Kryptolebias marmoratus)is one of two vertebrates known to employ both self-fertilization (selfing) and outcrossing. Variation in rates of outcrossing and selfing within and among populations produces individuals with diverse levels of heterozygosity. I designed an experiment to explore the consequences of variable heterozygosity across four ecologically relevant conditions of salinity and water availability (10‰, 25‰, and 40‰ salinity, and twice daily tide changes). I report a significant increase in mortality in the high salinity (40‰) treatment. I also report significant effects on fecundity measures with increasing heterozygosity. The odds of laying eggs decreased with increasing heterozygosity across all treatments, and the number of eggs laid decreased with increasing heterozygosity in the 10‰ and 25‰ treatments. Increasing heterozygosity also was associated with a reduction liver mass and body condition in all treatments. My results highlight the fitness challenges that accompany living in mangrove forests ecosystem and provide the first evidence for outbreeding depression on reproductive and condition-related traits.

Reducing the Extinction Risk of Populations Threatened by Infectious Diseases

Extinction risk is increasing for a range of species due to a variety of threats, including disease. Emerging infectious diseases can cause severe declines in wild animal populations, increasing population fragmentation and reducing gene flow. Small, isolated, host populations may lose adaptive potential and become more susceptible to extinction due to other threats. Management of the genetic consequences of disease-induced population decline is often necessary. Whilst disease threats need to be addressed, they can be difficult to mitigate. Actions implemented to conserve the Tasmanian devil (Sarcophilus harrisii), which has suffered decline to the deadly devil facial tumour disease (DFTD), exemplify how genetic management can be used to reduce extinction risk in populations threatened by disease. Supplementation is an emerging conservation technique that may benefit populations threatened by disease by enabling gene flow and conserving their adaptive potential through genetic restoration. Other candidate species may benefit from genetic management via supplementation but concerns regarding outbreeding depression may prevent widespread incorporation of this technique into wildlife disease management. However, existing knowledge can be used to identify populations that would benefit from supplementation where risk of outbreeding depression is low. For populations threatened by disease and, in situations where disease eradication is not an option, wildlife managers should consider genetic management to buffer the host species against inbreeding and loss of genetic diversity.

Homozygosity at its Limit: Inbreeding Depression in Wild Arabidopsis arenosa Populations

New combinations of genetic material brought together through hybridization can lead to unfit offspring as a result of outbreeding or inbreeding depression. In selfing plants such as Arabidopsis thaliana, outbreeding depression is typically the result of pairwise deleterious epistatic interactions between two alleles that can geographically co-occur. What remains elusive is how often alleles resulting in genetic incompatibilities co-occur in natural populations of outcrossing plant species. To address this question, we screened over two thousand five hundred wild Arabidopsis arenosa hybrid plants in search for potential genetic mismatches. We show that although abnormal deleterious phenotypes are common, the transcriptional profiles of these abnormal A. arenosa plants differ substantially from those seen in incompatible A. thaliana hybrids. The abnormal hybrid phenotypes in A. arenosa had different underlying genetic architectures, yet a repeated theme was increased homozygosity, indicating that inbreeding rather than outbreeding depression gives rise to some of the deleterious phenotypes segregating in wild A. arenosa populations.

Genetic Rescue and the Plight of Ponui Hybrids

Long-term sustainable and resilient populations is a key goal of conservation. How to best achieve this is controversial. There are, for instance, polarized views concerning the fitness and conservation value of hybrid populations founded through multi-origin translocations. A classic example concerns Apteryx (kiwi) in New Zealand. The A. mantelli of Ponui Island constitute a hybrid population where the birds are highly successful in their island habitat. A key dilemma for managers is understanding the reason for this success. Are the hybrid birds of Ponui Island of “no future conservation value” as recently asserted, or do they represent an outstanding example of genetic rescue and an important resource for future translocations? There has been a paradigm shift in scientific thinking concerning hybrids, but the ecological significance of admixed genomes remains difficult to assess. This limits what we can currently predict in conservation science. New understanding from genome science challenges the sufficiency of population genetic models to inform decision making and suggests instead that the contrasting outcomes of hybridization, “outbreeding depression” and “heterosis,” require understanding additional factors that modulate gene and protein expression and how these factors are influenced by the environment. We discuss these findings and the investigations that might help us to better understand the birds of Ponui, inform conservation management of kiwi and provide insight relevant for the future survival of Apteryx.

Selfing is the safest sex for Caenorhabditis tropicalis

Mating systems have profound effects on genetic diversity and compatibility. The convergent evolution of self-fertilization in three Caenorhabditis species provides a powerful lens to examine causes and consequences of mating system transitions. Among the selfers, C. tropicalis is the least genetically diverse and most afflicted by outbreeding depression. We generated a chromosomal-scale genome for C. tropicalis and surveyed global diversity. Population structure is very strong, and islands of extreme divergence punctuate a genomic background that is highly homogeneous around the globe. Outbreeding depression in the laboratory is caused largely by multiple Medea-like elements, genetically consistent with maternal toxin/zygotic antidote systems. Loci with Medea activity harbor novel and duplicated genes, and their activity is modified by mito-nuclear background. Segregating Medea elements dramatically reduce fitness, and simulations show that selfing limits their spread. Frequent selfing in C. tropicalis may therefore be a strategy to avoid Medea-mediated outbreeding depression.