Molecular genetics, evolution and phylogeography of bird species

Philip Morin and I were apparently the first to genotype birds noninvasively using feather pulp as a source of DNA (Publication 119). To date we have applied this methodology to two groups of threatened or endangered birds, loggerhead shrikes and hornbills. The former are found in California, the latter at my rainforest study sites in Thailand. To date, I have published 11 reports on this theme.

The San Clemente island loggerhead shrike is a critically endangered species; there were less than 10 breeding pairs left by the mid-1980s. Using noninvasive molecular genotyping methods, my postdoctoral fellow Nick Mundy and I have shown that the population on San Clemente island is different enough from those on other islands and the mainland to warrant saving. More interestingly, we have documented the loss of genetic variation in this population during the last century. Using DNA amplified from old museum skins (Publication 163) we found that the island population is only 60% as variable as the mainland population from which it was derived and it has lost 20% of its variation in the 80 years since 1915 (Publications 162 and 166). Four other papers have been published on aspects of molecular genetic variation in the shrikes. Graduate student, Lori Eggert and I have more recently extended the genetic survey to include the shrikes on the northern Channel Islands. We have confirmed and strengthened our original finding that San Clemente island loggerhead shrike has genetic integrity and merits conservation management (Publication 214).

We have published four papers on hornbill DNA sequence variation, phylogenetics and conservation (Publications 148, 170, 171, 172) but have not yet had the resources to undertake the necessarily extensive sequencing necessary to produce a molecular phylogeny.

We recently collaborated on an analysis of the genetic aspects of a recent avian colonization event involving juncos. Masters student Caylor Rasner employed microsatellite genotyping to elucidate the microevolutionary changes that have occurred in a small sedentary population of juncos that established an extralimital population on the UCSD campus about 20 generations ago (Publication 213).

I served as the external examiner of two Australian PhD theses that were based on the noninvasive avian genotyping methods I pioneered; studies of the powerful owl and the little penguin.

San Clemente loggerhead shrike. Captive breeding at the San Diego Zoo and reintroduction back onto the island brought this species back from the brink. Noninvasive genotyping established the merits of this remnant population (N = 14 at the low-point) as an evolutionarily significant unit. Photographed at CRES, San Diego Zoo.

Publications

148. Morin, P.A., J. Messier and D.S. Woodruff. DNA extraction, amplification and direct sequencing from hornbill feathers. Journal of the Science Society of Thailand 20:3141. (1994f).
Note: A methods paper with the first description of interspecific variation in Asian hornbills. Full collaboration between Woodruff and his former graduate students. Woodruff collected the feathers and directed the research. [No. of citations: 27]

154. Mundy, N.I., C.S. Winchell and D.S. Woodruff. Tandem repeats and heteroplasmy in the mitochondrial DNA control region of the loggerhead shrike (Lanius ludovicianus). Journal of Heredity 87:2126. (1996a).
Note: One of the first descriptions of these phenomena in birds. Full collaboration between Woodruff and his postdoc, Mundy; Winchell (Navy) facilitated tissue acquisition. [No. of citations: 41]

157. Mundy, N.I. and D.S. Woodruff. Polymorphic microsatellites in the loggerhead shrike isolated from a partial genomic library enriched for CA repeats. Molecular Ecology 5:811813. (1996d).
Note: Methods paper that permitted the remarkable 80-year retrospective analyses (Publication 166). Full collaboration between Woodruff and Mundy. [No. of citations: 35]

162. Mundy, N.I., C.S. Winchell and D.S. Woodruff. Genetic differences between the endangered San Clemente loggerhead shrike (Lanius ludovicianus mearnsi) and two neighbouring subspecies demonstrated by mtDNA control region and cytochrome b sequence variation. Molecular Ecology 6:2937. (1997a).
Note: Genetic comparisons helped characterize the endangered (N = 23) island subspecies and provided evidence for its reproductive isolation from mainland conspecifics even though the latter visit the island annually. Full collaboration between Woodruff and his postdoc, Mundy; Winchell (Navy) facilitated tissue acquisition. [No. of citations: 31]

163. Mundy, N.I., P. Unitt and D.S. Woodruff. Skin from feet of museum specimens as a non-destructive source of DNA for avian genotyping. The Auk 114:126129. (1997b).
Note: Methods paper that facilitated non-destructive genotyping of old museum specimens. Full collaboration between Woodruff and his postdoc, Mundy; Unitt (San Diego Natural History Museum) facilitated tissue acquisition. [No. of ISI citations: 60]

166. Mundy, N.I., C.S. Winchell, T. Burr and D.S. Woodruff. Microsatellite variation and microevolution in the critically endangered San Clemente loggerhead shrike (Lanius ludovicianus mearnsi). Proceedings of the Royal Society of London B 264:869875. (1997e).
Note: Major paper demonstrating that the island subspecies is half as variable as the mainland subspecies and has lost 20% of its variation in the last 80 years. Full collaboration between Woodruff and Nick Mundy; Winchell and Burr (Navy) facilitated tissue acquisition. [No. of citations: 45]

170. Woodruff, D.S. and S. Srikwan. Molecular genetics and the conservation of hornbills in fragmented landscapes. In: The Asian Hornbills: Ecology and Conservation. Thai Studies in Biodiversity. No. 2. Poonswad, P., ed. National Center for Genetic Engineering and Biotechnology (BIOTEC), Bangkok, Thailand, pp. 257263. (1998i).
Note: Review of conservation genetic principles and their application to conserving bird populations in fragmented rainforest patches. Full collaboration between Woodruff and his graduate student, Sukamol Srikwan.

171. Srikwan, S. and D.S. Woodruff. DNA sequence variation and hornbill conservation. In: The Asian Hornbills: Ecology and Conservation. The Asian Hornbills: Ecology and Conservation. No. 2. Poonswad, P., ed. National Center for Genetic Engineering and Biotechnology (BIOTEC), Bangkok, Thailand, pp. 6982. 336 pp. (1998h).
Note: Our second paper on the molecular phylogeny of hornbills included more African species and called some traditional views of relationships into question. Full collaboration between Woodruff and Srikwan. [No. of ISI citations: 2]

173. Mundy, N.I. and D.S. Woodruff. Conservation genetics of the San Clemente loggerhead shrike (Lanius ludovicianus mearnsi). Shrikes of the World - II: Conservation Implications. Proceedings of the Second International Shrike Symposium. International Birdwatching Center, Eliat, Israel. pp. 6063. (1998e).
Note: Review of the results of the first three years of our research on this endangered island endemic. Full collaboration between Woodruff and Mundy.

213. Rasner, C.A., P. Yeh, L.S. Eggert, K.E. Hunt, D.S. Woodruff and T.D. Price. Genetic and morphological evolution following a founder event in the dark-eyed junco, Junco hyemalis thurberi. Molecular Ecology 13:671681. (2004a).
Note: We describe the microevolution of a population of juncos on the UCSD campus; an extralimital population founded about 20 generations ago. My Masters student Caylor Rasner genotyped birds provided by Pam Yeh. Yeh was a doctoral student of Trevor Price and studied the colonists for five years; this paper reports the key result of her doctoral thesis. Undergraduate student Hunt assisted Yeh with sample acquisition. Graduate student Eggert assisted Rasner with the molecular methods. Price contributed the statistical analyses of the bottleneck. [No. of citations: 24]

214. Eggert, L.S., N.I. Mundy and D.S. Woodruff. Population structure of loggerhead shrikes in the California Channel Islands. Molecular Ecology 13:21212133. (2004b).
Note: Our earlier work had shown that the critically endangered loggerhead shrikes on San Clemente island were genetically isolated from conspecific mainland populations despite the occurrence on the island of overwintering birds from the mainland. Unfortunately our conclusion that the San Clemente island shrikes merited conservation was compromised by the US Navy, which had previously discouraged our study of birds from other Channel Islands. In the late 1990s the Navy reversed its position and facilitated our study of the birds on the northern Channel Islands. We were able to affirm our earlier conclusion that the San Clemente island birds were maintaining their genetic integrity despite occasional but genetically insignificant hybridization with birds of two other subspecies. We employ a new method involving Bayesian inference to apportion the genetic heritage of each individual bird studied among the three subspecies recognized in this area. Full collaboration between graduate student Eggert, former postdoc Mundy, and Woodruff. [No. of citations: 18]