High effective inbreeding coefficients correlate with morphological abnormalities in populations of South Australian koalas (Phascolarctos cinereus)

Abstract

Koalas have undergone a series of sequential founding events on islands in south‐eastern Australia in recent times. Populations in South Australia at the Eyre Peninsula and Mt Lofty Ranges were founded in the 1960s from a colony on Kangaroo Island. The Kangaroo Is. colony was derived from animals introduced to French Island from mainland Victoria over a century ago. In this study, we first use microsatellite markers to quantify levels of genetic variation within the South Australian koala populations and the relatively unperturbed Strzelecki Ranges population from mainland Victoria. This analysis revealed low levels of allelic diversity (1.7 ± 0.2 to 2.7 ± 0.5) and heterozygosity (0.208 ± 0.088 to 0.340 ± 0.110) in the three South Australian koala populations relative to the Strzelecki Ranges population, which has the highest levels of allelic diversity (4.7 ± 1.1) and heterozygosity (0.476 ± 0.122) in Victoria. Second, we measured the incidence of testicular aplasia, a unilateral or bilateral failure in testicular development, in the Eyre Peninsula and Kangaroo Is. populations, and in the ultimate founding population at French Is. Testicular aplasia was present at a frequency of 4.3% in French Is., 12.8% in Kangaroo Is. and 23.9% in the Eyre Peninsula, but was undetectable in the non‐bottlenecked Pilliga State Forest population of New South Wales. The incidence of testicular aplasia correlated positively with effective inbreeding coefficients derived from heterozygosity values (0.13 ± 0.06 in the Pilliga State Forest, 0.57 ± 0.17 in French Is., 0.63 ± 0.12 on Kangaroo Is. and 0.77 ± 0.12 in the Eyre Peninsula), which may indicate inbreeding depression. These findings are of concern when evaluating the long‐term conservation and viability of the South Australian koala populations, which may benefit from genetic augmentation in the future. Finally, unconfirmed reports suggested that animals from other states in Australia were introduced into the Mt Lofty Ranges population. Therefore, we quantified differentiation between the three South Australian populations and the Strzelecki Ranges and French Is. populations, based on microsatellites and mtDNA d‐loop region variation. R‐statistics and Goldstein's delta mu square distance revealed that differentiation at nuclear loci between populations paralleled known recent population history, except for the close relationship between Mt Lofty Ranges and French Is. This suggested a recent contribution to the Mt Lofty Ranges populations of animals derived from the French Is. translocation program. Furthermore, mtDNA d‐loop analysis found no evidence of contributions to the gene pool from animals of New South Wales or Queensland stock, implying that the population was derived exclusively from Victorian stock.

Oral health in South East Queensland Koalas: Prevalence of periodontal disease and other pathologies

“…Generational breeding should remove the occlusal errors if further evidence provides affirmation that the issue is genetic. This condition may be similar to the testicular abnormality related to inbreeding on Kangaroo Island, Eyre Peninsula and French Island (Cristescu et al, 2009, Seymour, 2001. Inbreeding in humans have produced orally related errors, particularly changes in tooth size (Niswander, 1975, Niswander andChung, 1965).…”

“…Genetic abnormalities from inbreeding have also been detected in Victoria and South Australian free ranging populations indicating that heterogeneity of the gene pool has diminished (Seymour, 2001, Cristecu et al, 2006. Recently the Environmental Protection and Biodiversity Conservation Act listed the species as vulnerable in New South Wales, Queensland, and the Australian Capital Territory (Anon, 2012).…”

Different portrayals of Koalas on Kangaroo Island: what gets whose attention (and what doesn't)

“…Koalas are reportedly capable of doubling their population every 2.5 to 3 years under optimal conditions (Martin 1997) and the KI population has been reported as having an overall fecundity of 79% (Robinson et al 1989). Studies examining genetic variability, and the knowledge that the koalas on the island were established from a small number of individuals, lead to the scientific definition of the koalas as "inbred" (Seymour et al 2001). Scientists took a wider view of the consequences of overabundance than most farmers, tending to emphasise the repercussions to the whole island's ecology.…”

Genetic consequences of isolation: island tammar wallaby (Macropus eugenii) populations and the conservation of threatened species

“…Small, isolated mainland populations face similar risks (Frankham et al 2002). Inbreeding and loss of genetic diversity are of particular conservation concern because they not only reduce fitness (Seymour et al 2001) and a species' ability to adapt and evolve to change, but increase the risk of extinction (Frankham et al 2002). The effects of genetic deterioration associated with inbreeding are known in both captive and wild populations (DeRose and Roff 1999;Hedrick and Kalinowski 2000), but have been poorly documented in island populations (Eldridge et al 1999).…”

“…Detailed studies can reveal the full cost of inbreeding depressions, but these are not always feasible. However there is evidence that inbred populations can sometimes manifest physical abnormalities such as cowlicks, kinked tails, cryptorchidism and poor sperm viability (Roelke et al 1993;Hedrick 1995;Madsen et al 1999;Seymour et al 2001;Sunquist and Sunquist 2001).…”