Inbreeding depression

The risk of inbreeding within fragmented lion populations is a fundamental problem in conservation biology [1] and although the problem has been clearly established, its impact has been greatly underestimated [2]. 

Although non-genetic causes of extinction through demographic and environmental stochasticity are sometimes claimed to be more important causes of extinction in wildlife than inbreeding [3-5], the response to these events by wild populations is ultimately impacted by loss of genetic variation [3,6].  As such, demographic and environmental stochasticity and inbreeding depression should be considered not as two independent causes of extinction but as factors operating interactively [7].

Increase in inbreeding levels for social animals is mostly determined by the number of social groups whilst the levels of unrestricted male dispersal as well as the variance in fecundity among social groups are also factors [7].

High levels of inbreeding can result in reduced genetic variation, low reproductive performance and increased cub mortality, as well as reduced immune competence [1-2, 8-9].  A lion population of 84 individuals in Hluhluwe- iMfolozi Park in South Africa displayed severe inbreeding depression and crashed to 20 native individuals and their offspring between 2002 and 2004 [1].  

It is commonly asserted that a population of 50 individuals of reproductive age is sufficient to avoid inbreeding depression short term [10-11], however this suggestion is based on captive populations [2]. Soulé [12] himself expresses concern regarding the use of this rule and reiterates that short-term survival criteria such as the "rule of 50" applies only to captive breeding, despairing that this rule has been misapplied to populations in nature.

Franklin [10] suggested that to retain evolutionary potential long term a population of 500 adults is required, and Lande [13] suggested 5000 was necessary. A genetic population model [7] to assess the rate of inbreeding depression in wild lions indicated a “continuous population of at least 50 prides, but preferably 100 prides, with no limits to dispersal” was required for genetically viable lion populations long term.  A minimum of 10 prides were predicted to be needed to avoid inbreeding depression short term.

Effective population size can be described as the ideal population size which would exhibit the same reduction in heterozygosity as that seen in the census size of a given population [14]. The definition of effective population size incorporates five assumptions; random mating, no migration, no mutation, no selection and non-over-lapping generations [15].  When a population violates any of these assumptions, its effective population size will differ from its census population [16]. Natural populations almost uniformly violate one if not all of these assumptions [17]. As such, the census population size is almost always greater than the effective population, often by several orders of magnitude.

It should be noted that the removal of individuals from a source population reduces the number of reproductive animals and therefore the annual recruitment of young animals [18].  Such action in a population near the threshold to avoid inbreeding depression risks could reduce annual recruitment below losses and instigate a decrease in the sub-population and thus increase the inbreeding risks.

In absence of data on effective or census populations, we estimated how many populations exist that could support the translocation and subsequent reintroduction elsewhere of individuals or prides without increasing the risk of inbreeding depression in the source population beyond acceptable parameters. Bjorklund [7] assumed an average pride size of 11.1 individuals.  The populations of the 86 IUCN identified Lion Conservation Units (LCU) were reviewed based on this pride size using minimum and maximum population estimates.  Where maximum population estimates were not provided estimates from Chardonnet’s [19] data was used to approximate the upper estimate.

Using maximum population estimates, only eight LCUs have sufficient prides (100) to be considered as potentially viable in the long term:  Chad / RCA (135 prides), Cuando Cubango (126), Greater Limpopo (282), Maasai Steppe (130), Okavango – Hwange (207), Ruaha – Rangwa (405), Selous (495) and Serengeti – Mara (315).  Of these, three are close to the threshold of 100 prides and further study of the actual rather than estimated effective population sizes should be conducted to confirm their status, especially in light of further reductions in lion populations since 2002 as reported by many countries.  When minimum population estimates are considered the Cuando Cubango and Maasai Steppe LCUs drop below the threshold leaving only five viable and one potentially viable population. 

The converse is that between 78 and 81 of the 86 LCUs are considered non-viable long term by published standards to avoid inbreeding and ensure evolutionary potential. Of these 53 are already considered non-viable in the short term and are areas where reintroduction programs could be beneficial.

References

[1] Trinkel M, Ferguson N, Reid A, Reid C, Somers M, Turelli, L, Graf J, Szykman M, Cooper D, Haverman P, Kastberger G, Packer C, Slotow R (2008)  Translocating lions into an inbred lion population in the Hluhluwe-iMfolozi Park, South Africa Animal Conservation 11: 138-143 (pdf)

[2] Frankham R (1995) Conservation Genetics.  Annual Review of Genetics 29: 305 – 27. (pdf)

[3] Caro TM, Laurenson MK (1994) Ecological and genetic factors in conservation: a cautionary tale. Science 263: 485 – 86. (pdf)

[4] Caughley G (1994) Directions in conservation biology.  Journal of Animal Ecology 63: 215 – 44. (pdf – purchase required)

[5] Lande R (1988) Genetics and demography in biological conservation.  Science 241: 1455 – 60. (pdf)

[6] Mills LS, Smouse PE (1994) Demographic consequences of inbreeding in remnant populations.  American Naturalist 144: 412 – 31. (pdf)

[7] Björklund M (2003) The risk of inbreeding due to habitat loss in the lion (Panthera leo).  Conservation Genetics 4: 515–523. (pdf – purchase required)

[8] Stein B (1999) Genetic variation and depletion in a population of lions (Panthera leo) in Hluhluwe-iMfolozi Park. MAgric thesis, University of Natal, Pietermaritzburg.

[9] Thornhill NW, ed. (1993) The Natural History of Inbreeding and Outbreeding:  Theoretical and Empirical Perspectives.  Chicago:  University of Chicago Press. 575 pp. (e-book)

[10] Franklin IR (1980) Evolutionary change in small populations.  In: Conservation Biology:  An evolutionary Ecological Perspective. (eds Soulé ME, Wilcox BA) Sinauer, Sunderland MA: pp. 135 – 49. (book – purchase required)

[11] Soulé ME (1980) Thresholds for survival: maintaining fitness and evolutionary potential.  In: Conservation Biology:  An evolutionary Ecological Perspective. (eds Soulé ME, Wilcox BA) Sinauer, Sunderland MA: pp. 151 – 70. (book – purchase required)

[12] Soulé ME (1987) Introduction pp. 1 – 9. In: Viable Populations for Conservation (ed. Soulé ME), Cambridge University Press: Cambridge. (e-book)

[13] Lande R (1995) Mutation and conservation.  Conservation Biology 9:782 – 91. (pdf -purchase required)

[14] Wright S (1978) Evolution and the genetics of populations. Volume 4. Variability within and among natural populations. University of Chicago Press, Chicago (e-book)

[15] Mace GM (1986) Genetic management of small populations. International Zoo Yearbook 24/25: 167-74. (pdf – purchase required)

[16] Crow JF, Kimura M (1970) An introduction to population genetics theory. Harper and Row, New York. (book – purchase required)

[17] Harris RB, Allendorf FW (1989) Genetically effective population size of large mammals: an assessment of estimators. Conservation Biology 3: 181-191. (pdf – purchase required)

[18] Smith JLD, McDougal C, Sunquist M (1987) Female land tenure system in tigers.  In: Tigers of the World: The Biology, Biopolitics, Management and Conservation of an Endangered Species (eds Tilson R, Seal US) Noyes Publications. (e-book)

[19] Chardonnet P, ed. (2002) Conservation of the African Lion: Contribution to a Status Survey. International Foundation for the Conservation of Wildlife, France & Conservation Force, USA.

Further Reading

Inbreeding and density-dependent population growth in a small, isolated lion population (pdf)
Trinkel M, Funston P, Hofmeyr M, Hofmeyr D, Dell, S Packer C, Slotow R (2010) Animal Conservation 13: 374-382

Case Study of a Population Bottleneck:  Lions of the Ngorongoro Crater (pdf)
Packer C, Pusey, AE, Rowley H, Gilbert DA, Martenson J, O’Brien, SJ (1991) Conservation Biology 5 (2): 219-230