Many species have experienced severe declines over the past two centuries as a result of growing anthropogenic pressures including direct exploitation, habitat destruction and climate change1,2,3. Some authors have even argued that Earth’s biodiversity is entering a sixth mass extinction event, characterised by the unprecedented loss of diversity at all levels4,5,6. Consequently, nowadays the persistence of many species is critically dependent on intensive management actions such as captive breeding, habitat restoration and reintroduction programs.
For many species, captive management has been the only option for survival7. For example, species like the Kakapo (Strigops habroptilus), Przewalski’s horse (Equus przewalskii) and giant Galapagos tortoise (Chelonoidis niger), among many others, would have gone extinct without human intervention and ex situ management8,9,10. Captive breeding is frequently used for the preservation of threatened species and, in some cases, for the rehabilitation of declining populations11,12,13,14. However, it can sometimes inadvertently lead to genetic or behavioural changes that are not always beneficial15. For example, when selective pressures in captivity differ to those that are usually encountered by a species in the wild, maladaptive alleles or behaviours can rise to high frequency in captive populations, which can compromise the survival of individuals after they are reintroduced into the wild16,17. Furthermore, in small captive herds, strong genetic drift and the increased probability of mating between close relatives can decrease heterozygosity and lead to inbreeding depression18,19,20,21,22. The fitness costs associated with inbreeding are manifest across taxonomic groups and include negative effects on litter size, longevity, female reproduction, male fertility and weight, in addition to hereditary defects23,24,25,26, all of which can have a strong impact on population viability.
Given that conserving genetic diversity and minimising inbreeding are important goals of most if not all captive breeding programmes27,28 and reduced genetic diversity has been associated with increased extinction risk and reduced adaptive potential29,30,31, knowledge of the effects of captive breeding on genetic diversity is crucial. However, genetic time-series data are still uncommon for both captive and wild populations32,33,34,35. Temporal data can be especially informative about changes in key genetic characteristics of a population such as allelic richness, heterozygosity and the effective population size (Ne); measures that reflect a combination of the speed of allele frequency change through genetic drift, the efficacy of selection and expected genetic diversity levels for selectively neutral loci36,37.
The pronghorn (Antilocapra americana) is the only extant species of the North American family Antilocapridae38,39. Pronghorns are thought to have been historically abundant, with documents from the 1800s suggesting that roughly 30–40 million individuals inhabited North America prior to the westward settlement of humans on the continent40,41. Nevertheless, current pronghorn numbers have been severely affected by habitat fragmentation and overhunting, with many populations having declined or disappeared entirely42,43,44. Nowadays, four pronghorn subspecies are recognized: the american pronghorn (A. a. americana), the sonoran pronghorn (A. a. sonoriensis), the peninsular pronghorn (A. a. peninsularis) and the mexican pronghorn (A. a. mexicana)45. The american pronghorn is the most widespread subspecies, with the sonoran, peninsular and mexican subspecies occupying more peripheral southerly areas40,45,44. Of these subspecies, the peninsular and sonoran are currently under national and international protection46,47,48. Overall, the pronghorn is one of the many species currently undergoing captive breeding and translocation, with breeding programs active in the USA and in Mexico49,50,51.
As with all of the pronghorn subspecies, wild populations of the peninsular pronghorn have declined substantially since the arrival of the fist Spanish settlers51. By the beginning of the twentieth century, the peninsular pronghorn was thought to number fewer than 1,000 individuals40. These numbers have since fallen to fewer than a hundred individuals in the 1980s42,51,52,53. In the face of imminent extinction, a captive breeding program for the peninsular pronghorn was established by the Peninsular Pronghorn Species Recovery Programme51. This commenced in 1997 at the Vizcaino Biosphere Reserve, Mexico, with 25 wild-caught adults and fawns being introduced to the breeding facilities during the first six years of the programme49. Since then, the captive population has grown rapidly.
Currently, the animals are held in three management stations, with an additional six small populations held by a consortium of zoos in the Southwestern USA53. The main conservation area encompasses over 54,000 ha located in two protected natural areas: the El Vizcaíno Biosphere Reserve and the Valle de los Cirios Flora and Fauna Protection Area. Some of the individuals are allowed to roam freely over the protected areas and are provided only with supplementary feeding and water during the dry season53. Other animals, mainly the breeding herd and pregnant females, are managed in smaller pens with year-round supplemental food and water. In 2018, a genetically informed selective breeding attempt was undertaken. A selection of young but sexually mature males and females were microsatellite genotyped (2018 cohort, this paper) and a breeding plan was developed that focused on minimizing the relatedness of the breeding partners. Animals with rare alleles were also prioritized for breeding in order to mitigate the loss of genetic diversity. Therefore, the peninsula pronghorn conservation program represents an example of successful ongoing species recovery, while also providing an opportunity to investigate the genetic outcomes of selective breeding.
Previous population genetic studies of pronghorns uncovered moderate to high levels of genetic diversity in the american subspecies45,54,55,56,57, while genetic diversity appears to be somewhat lower for the sonoran54,58 and peninsular pronghorn subspecies58,59. Moreover, the American subspecies shows little evidence of population genetic structure57 while population genetic differentiation at the subspecies level is more pronounced, revealing clear genetic discontinuities between geographically isolated populations58,59,35.
The reasons for the relatively low genetic diversity of the peninsular pronghorn subspecies are unknown, with two (non-mutually exclusive) explanations being possible. The first of these is that human induced habitat loss, competition with domestic animals and uncontrolled hunting may have caused the peninsular pronghorn to decline over the past three centuries51,44, which may have been further exacerbated by small population sizes and inbreeding over the past few decades of captivity. Alternatively, or additionally, dramatic ecological changes during the last glacial maximum (LGM; ca. 12,000 years ago) resulted in the desertification of most of the Baja California peninsula, reducing water availability60,61,62 and likely contributing to a gradual reduction in pronghorn numbers over thousands of years.
Here, we generated a time series dataset of multilocus microsatellite data for the captive peninsular pronghorn spanning the period 2009 – 2021 inclusive. We first evaluated changes in genetic diversity, heterozygosity and inbreeding over the past 13 years. We then used approximate Bayesian computation63 to evaluate support for alternative demographic scenarios that could explain the low genetic diversity of the peninsular pronghorn, and to estimate relevant parameters such as the current Ne and the strength and timing of historical declines. We hypothesised that the collapse of the peninsular pronghorn may have been driven by a combination of historical ecological changes and more recent anthropogenic factors. We furthermore hypothesised that, although the captive breeding programme has been successful in increasing the number of individuals, there may have been some unavoidable loss of genetic diversity and an increase in inbreeding over time, although we would expect that some of these changes will have been mitigated by the recent selective breeding attempt.