The fitness consequences of inbreeding in natural populations and their implications for species conservation (systematic map)
Threatened species often have small and isolated populations where mating among relatives can result in inbreeding depression increasing extinction risk. Effective management is hampered by a lack of syntheses summarising the magnitude of, and variation in inbreeding depression. Here we describe the nature and scope of the literature examining phenotypic/fitness consequences of inbreeding, to provide a foundation for future syntheses and management.
We searched the literature for articles documenting the impact of inbreeding in natural populations. Article titles, abstracts and full-texts were assessed against a priori defined criteria, and information relating to study design, quality and other factors that may influence inbreeding responses (e.g. population size) was extracted from relevant articles.
The searches identified 11457 articles, of which 614 were assessed as relevant and included in the systematic map (corresponding to 703 distinct studies). Most studies (663) assessed within-population inbreeding resulting from self-fertilisation or consanguineous pairings, while 118 studies assessed among-population inbreeding due to drift load. Plants were the most studied taxon (469 studies) followed by insects (52 studies) and birds (43 studies). Most studies investigated the effects of inbreeding on components of fitness (e.g. survival or fecundity; 648 studies) but measurements were typically under laboratory/greenhouse conditions (486 studies). Observations were also often restricted to the first inbred generation (607 studies) and studies frequently lacked contextual information (e.g. population size).
Our systematic map describes the scope and quality of the evidence describing the phenotypic consequences of inbreeding. The map reveals substantial evidence relating to inbreeding responses exists, but highlights information is still limited for some aspects, including the effects of multiple generations of inbreeding. The systematic map allowed us to define several conservation-relevant questions, where sufficient data exists to support systematic reviews, e.g. How do inbreeding responses vary with population size? However, we found that such syntheses are likely to be constrained by incomplete reporting of critical contextual information. Our systematic map employed the same rigorous literature assessment methods as systematic review, including a novel survey of study quality and thus provides a robust foundation to guide future research and syntheses seeking to inform conservation decision-making.
Genetic variation, Conservation genetics, Systematic review, Inbreeding depression, Outbreeding, Heterosis, Genetic load, Isolated populations, Small populations
The genetic diversity contained within threatened or endangered species is relevant to their conservation in a number of ways. First, many populations of these species are isolated and consist of small numbers of individuals. Such populations may have little genetic variation, and this could hamper their ability to adapt to changing or future environmental conditions through natural selection, reducing their potential to persist. A more pressing concern is that these small or isolated populations often consist of closely related individuals, and mating among these close relatives can lead to inbred offspring that suffer immediate health problems. This can act as an additional burden on the populations of endangered species, exacerbating other problems caused by lack of suitable habitat, exploitation and environmental change. Finally, similar problems can occur due to inter-mating between isolated and ecologically divergent populations. This may occur if human-aided movement of species brings previously separated populations into contact.
The study of these genetic risks and threats as applied to the conservation of wild species has become known as conservation genetics. Our aim here is to undertake a systematic synthesis and appraisal of one aspect of the large and growing literature on conservation genetics. This will enable us to understand whether we can draw general conclusions regarding the importance of genetic diversity to the sustainability of wild populations, and will assist in the integration of genetics knowledge and concepts into conservation. In particular we wish to understand where, and in which species, genetic problems are most likely to develop, with a view to establishing an objective and generic framework to better advise those responsible for species conservation.
This review deals with the impacts of inbreeding on fitness, and the threats to population persistence that this might incur. Inbreeding depression is a cost in fitness suffered by offspring of mating that has occurred among related individuals. This cost to fitness is caused when recessive genes that confer a detrimental phenotype are expressed in the homozygous state, or when benefits to fitness through heterosis are obviated (Keller and Waller, 2002, Hedrick and Kalinowski, 2000). Populations that are isolated in the landscape may be at particular risk of suffering adversely through inbreeding effects. This is because when such populations are small, or suffer a reduction in size, mating among relatives becomes more likely, and any genetic variation that is lost through drift cannot be replenished through migration. In other words the populations of greatest concern are thought to be those that are isolated from migration and have a low effective size.
It is important to note that inbreeding (and its associated cost) is a relative rather than an absolute measure (Keller and Waller, 2002). Inbreeding among relatives is always measured relative to a reference population. For example, the cost of inbreeding could be measured by experimentally self-fertilising individual plants and comparing the fitness of the resulting progeny to those derived from random mating within the same study population. The inbreeding coefficient of the inbred cross measures the extent of inbreeding relative to randomly mated individuals, which are defined as the unrelated reference population. Alternatively, one could measure the fitness of offspring within a single inbred population and compare this to the fitness of individuals arising from crosses between this and a separate population. This latter example includes cases of genetic rescue and heterosis where individuals within historically isolated and inbred populations can experience an increase in fitness after individuals from a neighbouring population are introduced.
Although inbreeding effects in natural populations have been reviewed (Hedrick and Kalinowski, 2000, Crnokrak and Roff, 1999, Keller and Waller, 2002), the existing syntheses need updating given the continued growth in the evidence base since these earlier publications. In addition, while one of these reviews is meta-analytic, none are systematic, and thus they may represent a biased view of the available evidence. Given this, there is a need for a new, up-to-date systematic review on this subject area, which can provide an overview of the evidence in order to assist species conservation. Furthermore, the relationship between neutral genetic variation within populations and the cost of inbreeding has not yet been investigated. There is a large body of evidence from molecular markers that documents this genetic variation within populations. It would be useful to know whether these studies contain any information that may be used to understand or predict the potential risks and magnitude of inbreeding effects in either species or their component populations. Therefore, in this systematic review our primary focus will be on the fitness costs of inbreeding in natural populations and the distribution of these effects across species with differing mating systems, life-histories and ecologies. As a secondary question, we will assess the relationship between the cost of inbreeding and levels of neutral variation retained within populations. The rationale for this secondary question is to ascertain whether variation measured with neutral markers captures information on effective population size and the purging of deleterious alleles that is relevant to inbreeding effects. We anticipate that our review has the potential to be useful to conservation, because it links species’ attributes that are easy to measure with fitness effects that could influence population persistence.