While some small populations have persisted against the odds, sufficiently large populations are generally needed to prevent eventual extinction (Halley et al., 2016). Small populations—which include species that have always had small populations and previously large populations that have been reduced to a few individuals—face three additional inherent and unavoidable pressures. These three additional pressures are: (1) loss of genetic diversity; (2) demographic stochasticity; and (3) environmental stochasticity and natural catastrophes. We will now examine how each of these pressures can lead a small population to eventual extinction. Much of this discussion is based on a ground-breaking manuscript by New Zealand ecologist Graeme Caughley, which discusses at length the threats faced by small and declining wildlife populations (Caughley, 1994).
Loss of genetic diversity
Species with high genetic diversity are generally more able to adapt to and reproduce under new conditions such as those brought by environmental changes. These adaptations can occur at both individual and population levels. For example, under climate change, some genes may allow some populations to adapt their ranges faster or better tolerate warmer and wetter environments, while phenotypic plasticity—the ability of one gene to express itself differently under different conditions—may allow certain individuals to better adapt to a changing environment. One species that displays remarkable phenotypic plasticity is the crystalline iceplant (Mesembryanthemum crystallinum); by regulating its photosynthetic pathways, an individual plant can adjust its water needs based on the amount of salt and moisture available in the environment (Tallman et al., 1997). Such flexibility may explain why this species, native to southwestern Africa, North Africa, and Europe, has been a successful invader in environments as diverse as those in South America, North America, and Australia.
While populations with many individuals usually also have high levels of genetic diversity, small populations regularly suffer from low levels of genetic diversity. This low genetic diversity not only leaves those populations unable to adapt to changing conditions, but also makes them more susceptible to a variety of deleterious genetic effects (Caughley, 1994). Each of these effects leads to even greater loss of fitness and genetic diversity, hence even larger population declines, and eventually extinction. In the next sections, we discuss further why these deleterious genetic effects are so harmful to small populations.
In wildlife populations, there are always some alleles that are relatively common, and others that are relatively rare. The relative abundance of any of these alleles may however change from one generation to another purely by chance. While common alleles generally tend to stay common, rare alleles have a high chance of being randomly lost in subsequent generations. Consider how each parent only passes on half of their genetic code to each offspring; this means that the ability of a rare allele to persist is dependent on how many individuals carry it, which individuals produce offspring, and how many offspring those individuals produce. Another important factor is population size (Figure 12.7.1): in any small population, only a limited number of individuals can carry any single allele, so the smaller the population, the higher the likelihood that alleles are lost to the next generation. This loss of alleles is called genetic drift.
While genetic drift equates to a loss of genetic diversity, there are some cases where populations show no obvious ill effects. Such may have been the case for female elephants in South Africa’s Addo Elephant National Park (Figure 12.7.2). Hunting once nearly killed off this entire population; by the time they were adequately protected in 1931, only 11 animals remained, eight of which were female. Of those eight females, at least four were tuskless, while only two, maybe three, females carried both tusks. Over the next decades, Addo’s female elephants have shown increasing degrees of tusklessness; by 2002, only 2% of females had tusks (by comparison, 96–98% of elephant females are normally expected to develop tusks, Maron, 2018). One can therefore postulate that the allele responsible for the tusk development in female elephants became rare, and that the progressive loss of tusked females is a sign of genetic drift (Whitehouse, 2002). While Addo’s female elephants do not show any known limitations from being tuskless, the loss of alleles can also be devastating to the population suffering from genetic drift if, for example, the lost allele(s) coded for traits that would have allowed a species to adapt to a changing environmental condition.
It is important to note that genetic drift is distinct from natural selection. That is, genetic drift involves random changes in the frequency of alleles, whereas natural selection involves changes in traits in response to sexual selection or specific environmental conditions. For example, reduced tusk size in some heavily-hunted elephants in Africa (e.g. Chiyo et al., 2015) is a selective pressure in response to hunting that favor large tusks—this is distinct from Addo’s female elephants that have lost their tusks even in the absence of selective hunting pressure.
Mating among closely related individuals, which occurs in small populations, often results in lower reproductive success and weaker offspring.
In large populations, a variety of instinctive mechanisms are in place to promote heterosis, which occur when offspring have a level of genetic variation that improves their individual evolutionary fitness. Some species are predisposed to disperse from their place of birth to prevent sibling–sibling or parent–offspring mating, while others are restrained from mating with close relatives through sensory cues such as individual odors. Many plants have morphological and physiological traits that facilitate cross-pollination and reduce self-pollination.
However, in small populations with few unrelated mates, the urge to breed might be stronger than the mechanisms that promote heterosis. Under these conditions, rather than forgoing reproduction, breeding among closely-related individuals (or inbreeding) can occur. This breeding among close relatives might result in inbreeding depression, which can occur when closely-related parents give their offspring two copies of a deleterious allele. Individuals suffering from inbreeding depression typically have fewer offspring or have offspring that are weak or fail to reproduce. Genetic studies have shown how birth defects in several small populations can be attributed to inbreeding depression (Xue et al., 2015). Inbreeding depression has also been identified as the reason why some small populations are more susceptible to diseases (Trinkel et al., 2011). Inbreeding depression can result in a vicious cycle for declining population sizes, where such declines can lead to even more inbreeding depression, and eventually extinction.
Large populations have many ecological, behavioral, and physiological mechanisms that prevent hybridization, the production of offspring among genetically distant taxa, whether they be individuals of different species, or individuals of the same species but with different adaptations (the latter being intraspecific hybridization). As with inbreeding depression, these mechanisms may fail in small populations, leading to outbreeding depression (Frankham et al., 2011). Because offspring that result from outbreeding depression have traits that are intermediate to their parents, they may not be adapted to either of the parents’ ecosystems. For example, one study found that plants suffering from outbreeding depression have weakened defenses against herbivory (Leimu and Fischer, 2010). Outbreeding depression may also lead to a breakdown in physiological and biochemical compatibility between would-be parents—hybrid sterility is a well-known consequence of this breakdown. Consequently, species and populations suffering from outbreeding depression often show similar symptoms to inbreeding depression, including lower fitness, weakness, and high rates of mortality.
The opposite of outbreeding depression is hybrid vigor. Under these conditions, the hybrid offspring can be quite strong in an evolutionary sense; they may even outcompete their parent species.
In some taxa, such as butterflies, annual plants, and amphibians, population size varies dramatically from generation to generation. During some years, populations can be so large that they appear to face little risk of extinction. However, abundant years can be misleading when followed by successive years of low abundance. Generally, in a population that undergoes extreme size fluctuations, the population size required to ensure continued persistence (i.e., the minimum viable population (MVP)) is in effect much nearer the lowest than the highest number of individuals in any given year. However, during years with low abundance, a phenomenon known as a population bottleneck may occur—that is, the small population size may lead to the loss of rare alleles from one generation to the next (Figure 12.7.3). Population bottlenecks may lead to more inbreeding depression which, in turn, reduces reproductive success (Heber and Briskie, 2010) and increases vulnerability to diseases (Dalton et al., 2016).
New populations founded by only a few individuals are vulnerable to a special type of population bottleneck, the founder effect. The founding individuals of a new population by definition start off with low genetic diversity, much less than the original population that the founders left behind. This low genetic diversity puts the new population at risk of further genetic diversity declines, which have lasting effects through time. This situation can occur naturally when only a small number of individuals disperse to establish a new population or when founder individuals come from a small population that already suffered from low genetic diversity. Being mindful of these concerns is especially important for translocation or captive breeding projects. For example, to prevent extinction of the world’s smallest gazelle, the Speke’s gazelle (Gazella spekei, EN), a captive population of this species, almost entirely restricted to Somalia, was established in the USA. The founder population for this captive breeding project consisted of only one male and three females, leading to severe levels of inbreeding depression and high mortality rates in offspring (Kalinowski et al., 2000). Understanding the importance of managing for genetic diversity can help avoid these and other challenges that can threaten the success of translocation projects.
Demographic stochasticity (also known as demographic variation) refers to random variations in a population’s demographic traits (e.g. sex ratios, birth rates, death rates), the cumulative effect of variation in individual organisms’ fitness. In any natural population, some individuals will produce fewer offspring than average, while others will produce more than average; some individuals will produce no offspring at all. Similarly, some individuals die younger than average, while others live longer than average. For populations that are sufficiently large, average birth and death rates provide relatively stable descriptions of key aspects of that population’s demography. However, when a population’s size decreases to below a certain threshold, variations in fitness of a small number of individuals can have a large impact on the overall populations’ demographic parameters, causing population size and other characters to fluctuate up or down unpredictably (Schleuning and Matthies, 2009). Consider, for example, an isolated population of crocodiles with only a few females. As with many other reptiles, offspring sex ratios of crocodiles are determined by the environmental temperature during incubation (Hutton 1987). If, by chance, the population experiences two years of high temperatures, which favor male offspring, and the few females die by chance, the all-male population may be doomed for extinction unless some female crocodiles immigrate from elsewhere.
The social systems of group-living animals can easily be disrupted when their population size or density falls below a critical level.
Environmental stochasticity and catastrophes
Environmental stochasticity, the unpredictable variation in environmental conditions, can cause dramatic population size fluctuations over time, and hence, substantially increase the risk of extinction. Consider, for example, how the development rate of many insects is strongly temperature-dependent (e.g. Rebaudo and Rabhi, 2018). In an average or warm year, young insects that hatch on time and feed well may result in ecologically fit adults that produce many young, whereas unusually cold years might reduce hatching success and larval activity, which could also reduce adult fitness (Gibert et al., 2001). So, highly unfavorable conditions in any one year can cause dramatic population declines, or even push a species to extinction if conditions persist over successive years across its range.
The increased risk of extinction from environmental stochasticity also applies to natural catastrophes that can occur at unpredictable intervals (e.g. droughts, storms, earthquakes, and fires). Range-restricted species are particularly vulnerable to this kind of threat.
Environmental stochasticity tends to increase the probability of extinction more than does demographic stochasticity. As discussed, this is especially true for small populations and range-restricted species.
The extinction vortex
As populations decline in size, they become increasingly vulnerable to the combined impacts from the loss of genetic diversity, inbreeding depression, Allee effects, environmental stochasticity, and demographic stochasticity. All these factors tend to lower reproduction, increase mortality rates, and reduce population size even more, in turn driving populations to extinction at increasingly faster rates over time (Fagan and Holmes, 2006). Conservationists sometimes compare this phenomenon to a vortex, spiralling inward, moving faster (or declining faster in the case of a population) as it gets closer to the center. At the centre of this extinction vortex (Gilpin and Soulé, 1986) is oblivion—the extinction of the species (Figure 12.7.4).