Introduction

Conservation science and evolutionary biology are twins. Both subjects were fertilized, developed, and emerged as neonates in the works of Charles Darwin. Among his contributions to conservation and evolution were two prescient suggestions that form the foundations of this Editorial. First, Darwin realized that small populations are more likely to disappear than are large populations (1859, p. 82): “Owing to the high geometrical rate of increase of all organic beings, each area is already fully stocked with inhabitants; and it follows from this, that as the favoured forms increase in number, so generally, will the less favoured decease and become rare. Rarity, as geology tells us, is the precursor to extinction. We can see that any form which is represented by few individuals will run a good chance of utter extinction…” He went on to suggest that one factor causing the extinction might be inbreeding (1859, p. 97): “When any species becomes very rare, close interbreeding [sic] will help to exterminate it; authors have thought that this comes into play in accounting for the deterioration of the Aurochs in Lithuania, of Red Deer in Scotland, and of Bears in Norway.” Second, was the concept that males and females follow different life-history trajectories guided by sexual selection (1871, p. 581): “The female has to expend much organic matter in the formation of her ova, whereas the male expends much force in fierce contests with his rivals, in wandering about in search of the female, in exerting his voice, pouring out odoriferous secretions, etc.…On the whole the expenditure of matter and force by the two sexes is probably nearly equal, though effected in very different ways and at different rates.”

The Allee effect

The Allee effect occurs when a species, or population, descends below a minimum threshold size and therefore faces a greater risk of extinction because the low number of individuals within the population results in decreasing population growth, or individual fitness (Angulo et al. 2018; Nagel et al. 2021; White et al. 2021; Witteman et al. 2016). The per-capita growth rate declines with fewer reproductive individuals, resulting in a downward spiral. Small populations can go extinct for multiple reasons, including a limited number of mates, insufficient numbers for cooperative hunting, protection, or rearing of offspring, drastic habitat changes and/or random fluctuations in demography. Social species are considered to be more prone to Allee effects because fewer individuals within groups means deceases in positive interactions that promote survivorship and reproduction (Angula et al. 2018). Allee effects can also change over time. Among Antarctic fur seals, Arctocephalus gazella, the primary cause of pup mortality shifted from starvation to predation across years (Nagel et al. 2021). In many mammalian species, dispersal by either males or females is a mechanism that reduces inbreeding (Clutton-Brock 2016). Sex-biased dispersal can minimize adverse genetic consequences of mating between kin.

Extinction can also arise from unpredictable and stochastic factors, another point noted by Darwin. He wrote (Darwin 1859, p. 68): “…with all beings there must be much fortuitous destruction, which can have little or no influence on the course of natural selection…a vast number of animals and plants, whether or not they be the best adapted to their conditions, mut be annually destroyed by accidental causes..” A case in point is the Puerto Rican parrot, Amazona vittata. A social frugivore residing nearly entirely in the El Yunque National Forest, Puerto Rico, their estimated population size was 13 individuals in 1973 (White et al. 2021). The population was subsequently enhanced through a captive breeding and re-introduction program which increased the number of parrots to a little over 50, when they were decimated: in September 2017, Hurricane Maria blew directly over Puerto Rico, devasting large parts of El Yunque, and eliminating the population of parrots.

Small populations may be at risk of extinction, but large populations are not immune. In his joint paper with Darwin describing natural selection, Alfred Russel Wallace (Darwin and Wallace 1859) suggested that food availability, not reproductive rate, could determine species abundance: “Perhaps the most remarkable instance of an immense bird population is that of the passenger pigeon of the United States, which lays only one, or at most two eggs…Why is this bird so extraordinarily abundant, while others producing two or three times as many young are less plentiful?…a constant supply of wholesome food is almost the sole condition requisite for ensuring the rapid increase of a given species, since neither the limited fecundity, nor the unrestrained attacks of birds of prey and of man are here sufficient to check it.” Unfortunately, the availability of “wholesome food” did not help the passenger pigeon; “unrestrained attacks” by human beings obliterated the passenger pigeon a little over a half century later. On 1 September 1914, the last passenger pigeon on the planet died at the Cincinnati Zoo (Barrow 2009). The total population had gone from possibly 2–5,000,000,000 birds to none in less than 60 years! A widespread population of billions of animals can be completely eliminated in a little over half a century.

Small populations and re-introductions

Conservation efforts are generally aimed at augmenting population sizes in order to avoid Allee effects. President Theodore Roosevelt, William T. Hornaday, Director of the Bronx Zoo, and Quanah Parker, a Comanche chief, were the first to demonstrate how captive breeding and re-introduction can save a species (Barrow 2009; Brinkley 2009; Gwynne 2010; Morris 2010). In April 1905, President Roosevelt met up with Parker in Oklahoma, USA, to go wolf hunting. After the hunt, the president shared an idea with Parker: How about helping to establish a protected wildlife area for a population of bison (Bison bison) in your backyard? Nearly 30 years had passed since Parker had been allowed to leave the Indian Reservation to go bison hunting. He spent months searching for bison before returning empty-handed to the Fort Sill Indian Reservation. On 11 October 1907, Hornaday oversaw the loading of seven bulls and eight cows from the Bronx Zoo bison collection into a special railroad car. Seven days later, Quanah Parker greeted them. The bison were transferred to wagons for the 12–13-mile trip to the Wichita Forest and Game Preserve, where they were released. The area is now called the Wichita Mountains Wildlife Refuge and is home to about 650 bison. The re-introduction was ignited by Hornaday’s fear that unless bison could be bred in captivity and re-introduced to their native habitat, they would go extinct in the wild (Hornaday 1889). He had estimated their numbers at over 40,000,000 in the 1800s, and by the turn of the century, less than 300 were in the United States of America.

Since 1907, a number of breeding and re-introduction programs have been spearheaded by zoos and successfully saved species by bringing them back to their native habitat. Among the key success stories are the California condor (Gymnogyps californianus), black-footed ferret (Mustela nigripes), and Arabian oryx (Oryx leucoryx), which suffered a dangerous setback when the re-introduced population was devastated by the illegal wildlife trade and the 1990 Gulf War (Miranda et al. 2023). In addition, the pioneering work of primatologist Devra Kleiman resulted in the first successful re-introduction of a primate to its natural habitat when golden lion tamarins (Leontopithecus rosalia) were returned to the Atlantic Forest in Brazil (Kleiman 1989). Re-introduction programs often begin, out of necessity, with a limited founding population.

Inbreeding and genetics in the wild

One commonly suggested reason for why a small population with a limited distribution is more at risk of extinction than a large population occupying a diverse landscape is that genetic factors, such as inbreeding depression, genetic drift, or a high mutation load, are detrimental to population survival and, as a consequence, animals have evolved mechanisms to avoid incest or inbreeding. Frankel and Soulé (1981) reasoned that conservation and evolution are connected by genetics because species survival is influenced by genetic diversity, which is mediated by bottlenecks, population demography and size, and reproductive output, or fitness. They suggest that population adaptations are reduced by inbreeding depression and/or genetic drift, which can result in a loss of population fitness due to decreased heterozygosity, leading to extinction. However, the detrimental consequences of inbreeding might not be apparent if populations have already eliminated deleterious recessive alleles. A compressed population size can only result in inbreeding depression or loss of fitness if at least one reproductively active male and one reproductively active female harbor the exact same deleterious allele(s) and mate with each other and produce either stillborns, non-viable offspring, or those who are infertile as a consequence of their inheritance of those deleterious alleles.

Among mammals, as far as I am aware, only one species in the wild fits this description; the grey wolf, Canis lupus, of Isle Royale National Park, Minnesota. In the winter of 1948, probably no more than two or three wolves crossed an ice bridge from Canada to Isle Royale (Robinson et al. 2019; https://www.nps.gov/isro/learn/nature/wolves.htm). The population peaked at about 50, but suffered a severe crash when a domestic dog introduced a virus, such that only 11 wolves were counted in 1989 (https://www.nps.gov/isro/learn/nature/wolf-moose-populations.htm). A re-introduction program was initiated and the population recovered to 30 wolves in 2005, then declined to only two in 2015. The population has since rebounded slightly as a result of a continuing re-introduction program. The wolves on Isle Royale display a high level of inbreeding, as revealed in their genome structure with large runs of homozygosity (ROH), a sign of identity by descent through maternal and paternal lineages (Robinson et al. 2019). Their morphology is also indicative on high inbreeding, for example, vertebral anomalies. In this case, the founding population was less than five individuals. Had re-introduction not occurred, the small population would have gone extinct with inbreeding as the leading culprit.

In natural populations of mammals, mating between relatives has been recorded, but levels of inbreeding based upon genetic assessments are low. Among yellow baboons (Papio cynocephalus) living in Amboseli National Park, Kenya, levels of inbreeding are minimized due to sex differences in life-history profiles (Galezo et al. 2022). About half of the females die before reaching the median age of first birth (5.95 years; Alberts 2019). Baboon interbirth intervals can be influenced by dominance rank, body condition, available resources, age, group size, and parity (Strum and Western 1982; Gesquiere et al. 2018), but on average a surviving infant is produced every 1.75 years from primiparity to death (Gesquiere et al. 2018), resulting in about 4–5 surviving progeny. For male baboons, 44% die before reaching the median age when they can mate-guard sexually receptive females (7.7 years; Alberts 2019). Of those that survive, adult male baboons follow an age-related reproductive output pattern, with offspring production peaking between 9 and 11 years of age, concurrent with the period when males occupy high rank (Silk et al. 2020). By the time a male is 12 years old, the probability of siring offspring is close to zero, even if he survives for a few years beyond that time (Silk et al. 2020). Female baboons remain in their natal troop for their whole lives, while males might disperse to non-natal troops one or more times.

Male dispersal and reduced life expectancy combine to limit matings between kin. Only 1% (6/607) of offspring were born to known relatives and close to 80% of mother–son dyads could not mate because life-history trajectories eliminated co-residency. Maternal kin mate with each other less than paternal kin, suggesting that factors other than degree of relatedness influence reproductive behavior. Female savanna baboons (P. anubis) in Gilgil, Kenya, copulate with natal males, but prefer new immigrants, who tend to be both young and enter at high rank (Bercovitch 1991, 1995). Female preference for newcomers was hypothesized (Bercovitch 1991, 1995) to have evolved not as an incest-avoidance mechanism, but as a means of increasing offspring survivorship because immigrant males are more likely to remain in the troop and males form bonds with infants that they have probably sired. Subsequent paternity analyses in multiple populations of baboons have supported this hypothesis by revealing that male associations with, and protection of, infants (Fig. 1) are a form of paternal care that can boost immature baboon survivorship (Buchan et al. 2003; Silk et al. 2020; Städele et al. 2021).

Fig. 1
figure 1

© Fred Bercovitch

An adult male protecting an infant by using an eyelid flash as a threat to a conspecific. The young baboon is hiding behind the right leg of the adult male. Photo

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The founding group of the rhesus monkey (Macaca mulatta) population on Cayo Santiago, Puerto Rico, consisted of 409 individuals captured in 12 locations in India and brought to the island in 1938 (Rawlins and Kessler 1986). In a longitudinal study covering 30 years, Bercovitch and Berard (1993) found that females produce first offspring when 4–6 years of age, with 90% of them starting when 4 years old. Rhesus macaques breed seasonally, and the average interbirth interval is approximately 1 year (Rawlins and Kessler 1986). Females can produce up to 12 surviving young, but the average number is 4–5 (Fig. 2; Bercovitch and Berard 1993).

Fig. 2
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© Fred Bercovitch

An adult female golden monkey nursing her non-golden offspring. The etiology of the golden phenotype is unclear. See Kessler et al. (1986) for details. Photo

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Among male rhesus on Cayo Santiago, the average age at first sirehood is 7.5 years, but over a 10-year period 48% of males produced no young (Bercovitch et al. 2003). Rhesus macaque males have an age-related inverted “U”-shaped reproductive output, peaking between 9 and 11 years of age (Fig. 3) with an exceptionally pronounced reproductive skew (Widdig et al. 2004). Six males were responsible for siring 80% of infants over a 6-year period. Seventy-five years after their introduction to Cayo Santiago, the rhesus population showed no evidence of inbreeding depression, despite the male reproductive skew and the fact that no new monkeys had been brought to the island since the initial cohort (Widdig et al. 2017). A genetic pedigree analysis of close to 3000 monkeys found that 92.4% of mating pairs were unrelated, and among related monkeys, maternal kin were more likely than paternal kin to breed together (Widdig et al. 2017). In his field study of rhesus macaques in northern India, Lindburg (1971, p. 65) did not record males fighting for estrous females, but found that: “Formation of a sexual relationship was in some cases a result of the initiative of the female. Some males resisted these solicitations by threatening, particularly in the early stages of female receptivity.” Although observed fights among males are infrequent (Fig. 4), among the Cayo Santiago rhesus macaques, male injuries are more prevalent during the mating season, the risk of injury is inversely related to dominance rank, and injuries can result in death (Pavera-Fox et al. 2022). Female mate choice for novel males among Japanese macaques (M. fuscata) might be one factor mediating male dispersal (Huffman 1991). Continuous mount rejection by female Japanese macaques was associated with male troop tenure. As with baboons, males are the dispersing sex while females remain in their natal troop for their entire lives. Sexual bimaturism in baboons and rhesus monkeys contributes to the infrequency of co-resident adult kin of the opposite sex.

Fig. 3
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Age-dependent reproductive success of male rhesus macaques living on Cayo Santiago over a 6-year period. See Widdig et al. (2004) for a detailed explanation

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Fig. 4
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© Richard G. Rawlins

An adult male rhesus macaque displaying his formidable canines. Photo

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Six years before the macaques were brought to Cayo Santiago, 107 Soay sheep (Ovis aries) were introduced to Hirta Island, Scotland (Stoffel et al. 2021). Using a genome analysis of long rows of heterozygosity (ROH) to determine inbreeding coefficients of 5952 sheep over a 35-year period, Stoffel et al. (2021) could not determine fitness consequences for individuals resulting from inbreeding, but they found that the average inbreeding coefficient was quite high and that lamb mortality rate exceeded 50%. However, the population size on Hirta has undergone a number of density-dependent fluctuations over time, mortality among lambs ranges across years from 10 to 90%, with a primary cause of mortality being rainfall (and cold temperatures) in March (Catchpole et al. 2000). Hence, despite the small number of founders, geographical isolation, relatively high inbreeding coefficient, and sometimes-high lamb mortality rate, the population has continued to thrive over the last 90 years.

Unlike baboons, rhesus monkeys, and Soay sheep, banner-tailed kangaroo rats (Dipodomys spectabilis) are solitary and regularly give birth to litters, not singletons (Willoghby et al. 2019). However, like baboons and rhesus macaques, maternal kin are less likely to mate with each other than paternal kin, and both dispersal and mate choice appear to minimize inbreeding levels. Willoughby et al. (2019) examined the genetic profile of 1441 kangaroo rats in southeast Arizona, and concluded that the inbreeding coefficient was quite low (0.07). They reported that inbreeding coefficients correlated negatively with lifetime reproductive success (LRS), but inbreeding contributed less than 5% to the variance in LRS.

As noted earlier, California condors are a successful re-introduction story. From an estimated effective population size of 50,000 individuals around 1 million years ago, numbers plummeted to 22 in 1982 (Robinson et al. 2021). Despite the extremely small founding population size, these birds have a very high degree of genetic diversity and their current population is around 500 individuals, with 60% of them flying in their natural habitat (Robinson et al. 2021).

Both the northern white rhinoceros (NWR; Ceratotherium simium cottoni) and the southern white rhinoceros (SWR; C. s. simium) underwent severe population bottlenecks beginning around the end of the 19th century due to human hunting. However, they experienced completely opposite population trajectories afterwards, with the former plunging but the latter soaring (Sanchez-Barreiro et al. 2021). The NWR used to range from northern Zambia to southern Sudan, probably numbering tens of thousands of individuals, but their number decreased to around 2400 in 1960, about 350 in 1984, and now only two, both elderly, non-fertile females, are alive in Africa today (Emslie 2020; Sanchez-Barreiror et al. 2021). The SWR used to range from south of the Zambezi River to the southern parts of South Africa, possibly numbering several hundred thousand individuals, declining to fewer than 50 isolated in a small enclave in Kwa-Zula, South Africa, but ballooning to approximately 18,000 individuals now living in their historical range in Africa (Emslie 2020). Despite the antithetical pathways, the two subspecies underwent identical genetic changes. Genome-wide heterozygosity decreased and inbreeding coefficients based upon ROH increased when comparing pre-bottleneck specimens (obtained from museums) to post-bottleneck specimens (Sanchez-Barreiror et al. 2021). However, even though the SWR population fell below 50 animals, the subspecies genetic load is no different now from that estimated from their pre-bottleneck period.

To summarize, inbreeding occurs in wild populations of baboons and kangaroo rats, in island populations of rhesus monkeys and Soay sheep, and in re-introduced populations of condors and rhinoceros. However, none of these populations are characterized by inbreeding depression or reduced population fitness due to kin mating. Where genetic relatedness has been established, evidence shows that close kin (i.e., r > 0.25) rarely mate. Whether this pattern is due to females not soliciting mating from closely related males or males not attempting to mate guard and copulate with closely related females has not been subject to detailed study.

Genetic heterogeneity is maintained, even in populations with a limited distribution, by processes including natal dispersal, mate choice, and sex differences in life history profiles. Sex-biased dispersal, as well as male and female mate selection, could have evolved as a means of increasing diversity among progeny rather than a way of avoiding incest. Whether or not genetic diversity favors adaptability to changing environments has been questioned (Teixeira and Huber 2021), but maximizing genetic heterogeneity by saving ecosystems and populations is a recipe that can, at a minimum, prevent species from getting sucked into an ‘extinction vortex’ (Gilpin and Soulé 1986).

Conclusions

The major threats noted on the IUCN Red List for many primate and non-primate species (e.g., giraffes, African elephants (Loxodonta)) do not include inbreeding depression but are associated with human activities (i.e., habitat loss/degradation/fragmentation, poaching, climate change, human population growth). Humans have been wiping out species since the Pleistocene Ice Ages (Braje and Erlandson 2013). A review comparing IUCN Red List classification with the extent of genome-wide nucleotide diversity across species found no association between threat level and genetic diversity (Teixeira and Huber 2021).

As a consequence of sex differences in life-history strategies, inbreeding is kept to a minimum. Given male–female differences in development, reproduction, and residency patterns, among savanna baboons, rhesus macaques, as well as other species of non-human primates, most siblings are unlikely to have shared paternity. Genetic heterozygosity among female rhesus macaques is associated with sociality by increasing the extent of grooming and decreasing the level of aggression received (Charpentier et al. 2008), and sociality promotes longevity and infant survivorship in baboons (Cheney et al. 2016; Silk et al. 2009). Evolution has molded a pattern that maximizes genetic heterozygosity among offspring of iteroparous mammals, which could favor individual adaptability to changing socioenvironmental conditions while minimizing inbreeding between close kin, thereby reducing the chances of maintaining a high genetic load and producing offspring that do not survive. Regardless of whether an animal’s ‘motive’ is incest-avoidance or diversity of offspring genomes, population crashes as a consequence of inbreeding are exceptionally rare, with the only solid case among mammals involving a founding population of fewer than five wolves.

In koalas, Phascolarctos cinereus, successive joeys tend to be sired by different males (Ellis et al. 2002) and I predict that a similar pattern occurs in primates. Having opened with two of Darwin’s insights, closing with one more is appropriate. He wrote: “…females often prefer strangers to their old companions” as mates (Darwin 1882). He also commented (1871, p. 738): “There is even reason to suspect, improbable as this will at first appear, that some males and females of the same species, inhabiting the same district, do not always please each other, and consequently do not pair.”, which could result in an Allee effect. The search for novel mating partners within and between groups of populations of animals could be at the heart of both maximizing fitness and indirectly reducing vulnerability to species extinction. Conservation of biodiversity requires the protection of ecosystems in which animal behavioral and ecological flexibility evolved to enable individuals to convert food into offspring. Males and females do this by following sex-specific life-history patterns that yield the genetic population structure of (meta) populations that become the forebears of succeeding generations.