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Discussion
Does the divided infraorbital foramen diagnose the Asian lion?
next sectionTwo lions from Iran have DIF (Appendix 1), contradicting the hypothesis that DIF distinguishes the skulls of Indian lions from Gujarat, from not only those of all other lions, including other Asian lions, but also from those of all other felids (O’Brien et al., 1987). Although our results show that DIF is not exclusive to the Gir Forest lions, it can be confidently reported that DIF rarely appears in sub-Saharan African lions, which, on the basis of a molecular phylogeny, are likely to be ancestral to the North African -Asian population (Barnett et al., 2006a). Also, our results suggest that the extinct North African Barbary lion does not seem to have DIF, at least at a high frequency. Furthermore, it is suggested based on maternally inherited mitochondrial DNA, that the modern lion does not appear to have hybridised with the extinct northern Holarctic lions of the Pleistocene, including the European cave lion (Burger et al., 2004; Barnett et al., 2009), where 13% have DIF. Therefore, a higher DIF frequency in the Asian population may be a characteristic that developed after the lion colonised Asia, potentially reflecting the recent colonisation history of the lion. These arguments suggest that the higher frequency of DIF in Asian lions is still an important morphological feature that distinguishes their skulls from those of African lions, even though we now know that some African individuals have it.
Divided infraorbital foramen and past bottlenecks
Todd (1965) speculated that the degree of expression and/or penetrance of DIF are under the influence of only a few polygenes, which have shown shifts in frequency in the Indian lion population, possibly due to genetic drift. As the phylogenetic ancestor of the Asian lion (i.e. the sub-Saharan African lion: Barnett et al., 2006a) does not show a high prevalence of DIF, has the Asian lion experienced any severe population/genetic bottleneck in the past, where genetic drift (and/or founder effect) could have been a major factor influencing the frequency of occurrence of the population’s genetic and morphological characteristics? Driscoll et al. (2002) suggested, based on an analysis of 88 nuclear microsatellite loci, that the extreme genetic homogenisation in the current Gir Forest lion population results from a population genetic bottleneck around 1,100 - 4,300 years ago, which was probably caused by natural events.
A more recent, and probably human-caused, population bottleneck appears to have been most severe at the end of the 19th century when it was estimated that ‘no more than ten or a dozen’ individuals survived (Fenton, 1909; Kinnear, 1920; Wynter-Blyth and Dharmakumarsinhji KS, 1949; Dharmakumarsinhji and Wynter-Blyth, 1950; Talbot, 1960), although the severity of this bottleneck may have been exaggerated (Srivastav and Srivastav, 1997; Divyabhanusinh, 2005). Todd (1965) analysed the temporal change in frequency of DIF in Indian lions – DIF occurred in 85% (4/5) of Indian lion skulls collected in the 19th century, and 60% (6/10) of early 20th century skulls (pre-1950: 1910-1931), whilst only 27% (5/18.5: Todd (1965) gave the broken specimen (Mumbai 1261: Appendix 1) 0.5) had DIF in post-1950 specimens. Our results based on a larger sample indicate that DIF occurs in 45% (5/11) of Indian lion skulls collected in the 19th century, which rises to 67% (10/15) in the early 20th century (pre-1950, including those without recorded collecting dates yet likely to have been collected during this period as indicated by from their museum register numbers), but this falls to 38% (11/29) post-1950. There is no detectable significant differences in prevalence of DIF between these periods, and therefore the results do not support the previous hypothesis that there have been considerable shifts in DIF frequency over the past 200 years (Todd 1965). Granted, the combined sample size is still small, and there is a possibility that the sample is not a fair representation of the population. Also, we emphasise that there is a marginally statistically significant difference between pre-1950 and post-1950 samples, which may be strong enough for scientists to further investigate this issue. In other words, it may be possible that the recent anthropogenic population bottleneck and subsequent population increase (Nowell and Jackson, 1996) have influenced the prevalence of this population-specific characteristic of Asian lions. The foregoing arguments suggest that, although the shift may not be as dramatic as Todd (1965) speculated, conservationists may need to monitor carefully the morphological characteristics of the Asian lion both in the wild and in captivity. Captive breeding programmes for the Asian lion in Europe and India provide a unique opportunity to study the inheritance of DIF and other morphological characteristics in the Asian lion, in order to better understand changes in the prevalence of these characters in historical wild populations.