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Population-Genetic Structure of a Philopatric, Colonially Nesting Seabird, the Short-Tailed Shearwater (Puffinus Tenuirostris)

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Population-Genetic Structure of a Philopatric, Colonially Nesting Seabird, the Short-Tailed Shearwater (Puffinus Tenuirostris) The Auk 111(1):70-79, 1994 POPULATION-GENETIC STRUCTURE OF A PHILOPATRIC, COLONIALLY NESTING SEABIRD, THE SHORT-TAILED SHEARWATER (PUFFINUS TENUIROSTRIS) JEREMYJ. AUSTIN, ROBERTW. G. WHITE, AND JENNIFERR. OVENDEN Departmentof Zoology,University of Tasmania,GPO Box252 C, Hobart, Tasmania 7001, Australia ABSTl•CT.--Short-tailedShearwaters (Puffinus tenuirostris) are a numerous,colonially nest- ing seabird that is strongly philopatric. We applied restriction-enzymeanalysis of mito- chondrial DNA (mtDNA) to 335 individuals from 11 colonies across southeastern Australia to assesspopulation-genetic structure and the amount of genetic variability in this species. Eleven 6/5.33-baseand four 4-baserestriction enzymes revealed 25 and 48 mtDNA haplotypes in two overlapping surveysof 215 individuals from seven coloniesand 231 individuals from eight colonies,respectively. A low mean sequencediversity among individuals (0.247%)and lack of spatialstructuring of mtDNA haplotypessuggest a lack of population-geneticstructure and a reduced ancestralpopulation size during glaciation, followed by a population and range expansion.Intracolony mtDNA diversitiesin three recently establishedcolonies and in one colonythat hasexperienced a recentbottleneck were comparableto mtDNA diversities within larger and older colonies.This suggeststhat, despite strictphilopatry in thosecolonies, colony founding and recovery from population reduction occursvia immigration of a large number of individuals. Received27 April 1993,accepted 11 November1993. DIRECT(genetic) and indirect (observational) is highly polymorphic among individuals (Av- estimates of the type of genetic-population ise et al. 1987). Maternal inheritance and hap- structure within a species often can produce loid transmission result in an effective popu- conflicting results (Moum et al. 1991, Avise et lation size for the mitochondrial genome about al. 1992, Birt-Friesen et al. 1992). Evidence from one-quarter of that for nuclear genes. Mito- band returns suggeststhat many bird species chondrial genes, therefore, are more sensitive exhibit strong natal philopatry to a particular to the effects of random genetic drift, founder site or region. Based on this indirect evidence, events and bottlenecks than are nuclear genes Quinn and White (1987) suggestedthat genetic (Birky et al. 1983). Direct estimatesof the type differentiation among populationsof philopat- of genetic structure of populations, based on ric speciesmay be substantialas a consequence the geographic distribution of extant mtDNA of limited gene flow. However, indirect meth- haplotypesthat retain a phylogeneticrecord of ods are limited in terms of the number of col- population connectednessand historical de- onies (space) and the number of years (time) mographic changes, therefore, reflect past as from which data can be collected. These meth- well as contemporary gene flow. ods, therefore, can often fail to detect rare, but The Short-tailedShearwater (Puffinus tenuiro- evolutionarily important, events such as large- stris),or muttonbird, is a colonially nesting sea- scaledemographic changes and episodicor con- bird breeding on islands and headlands along tinuous, low-level dispersal that can affect the the southern coastline of Australia. Population genetic structuringof populations(Slatkin 1987, size is estimated to be 23 million breeding birds Avise et al. 1992). with numbers concentrated around Tasmania Analysisof mitochondrial DNA (mtDNA) has and the islands of BassStrait (Skira et al. 1985). proved to be an informative and useful method Although Short-tailed Shearwaters are trans- for examining population-geneticstructure in equatorialmigrants, long-term banding studies a variety of organisms,including birds (Ball et suggeststrong philopatry, with only limited na- al. 1988, Ovenden et al. 1991, Avise et al. 1992, tal dispersalto adjacentcolonies (Wooller et al. Birt-Friesen et al. 1992). Evolution of mtDNA 1990). For example, of 23 banded adults found is more rapid than for nuclear DNA (Brown et in a survey of 4,573 birds breeding on Little al. 1979)and the nucleotidesequence of mt DNA Green Island in BassStrait during 1988, 17 had 70 January1994] Geneticsof Short-tailedShearwaters 71 been banded on Little Green Island as adults or nestlings, 3 as nestlings on Great Dog Island, and 3 as surface adults on Fisher Island (Skira pers. comm.). The latter two colonies are less than 5 km from Little Green Island. In addition, approximately73,000 individuals were banded at various colonies in Victoria, New South Wales (NSW), South Australia and elsewhere in Tas- mania over 18 years, but none have been re- covered in a number of large surveyson Little Green Island or in annual surveys on Fisher Island (Serventy and Curry 1984). Populations of the Short-tailed Shearwater have experienced considerable flux within the last 15,000 years. Most current breeding sites would have been unsuitablebreeding habitat during the last ice age, when the sea level was at least 100 m lower than it is today (Milliman and Emery 1968); thus, these sites must have -45os been colonized within the last several thousand years. Prior to European settlement (ca. 1800), 140 øE 145øE 150øE Aborigines in Tasmania harvested eggs and chicksduring the breedingseason for food(Ryan Fig. 1. Locationsof breeding colonies of Short- tailed Shearwaters(approximate size in parentheses): 1981). Subsequently, shearwatershave formed (1) WhalebonePoint (3,000burrows; Naarding 1980); the basisof a muttonbird industry with up to (2) Cape Direction (20,000burrows; Naarding 1980); one million chicks taken each year for their (3) CapeDeslacs (20,000 burrows; Naarding 1980);(4) meat, feathers and oil (Skira et al. 1985). In the Trial Harbour (15,000 burrows;Naarding 1980);(5) last 100 years many new colonies have been Little GreenIsland (150,000 burrows; Naarding 1980); established both within and outside the histor- (6) GreatDog Island (375,000pairs; Skira et al. 1985); ical range of the species,representing both a (6) Port Fairy (52,100 burrows; Harris and Norman major range, and possiblepopulation, expan- 1981); (8) Cape Woolamai (356,000 burrows; Harris sion (Davies 1959, Harris and Bode 1981). In- and Bode1981); (9) DoughboyIsland (2,000burrows; dividual colonies have become extinct, fluctu- Harris and Norman 1981);(10) Gabo Island (30,000- 40,000pairs; Reilly 1977);(11) Montague Island (15,000 ated in size, and suffered severe bottleneck pairs;Lane 1979).Dots on map inset indicatepositions events (Gilham 1962, Harris and Bode 1981). of coloniesat extremesof breedingrange. We applied restriction-enzyme analysis of mtDNA to examine the population-genetic natal origins of capturedbirds. This could pro- structure of Short-tailed Shearwaters,repre- vide valuableinformation on the relationship senting1 ! distinctnesting colonies, throughout betweenbirds during migrationand foraging, southeasternAustralia. We included one colony on wintering grounds,and during the breeding that had been subjectedto a recentpopulation season.In addition, the natal origins of found- bottleneck (Gabo Island) and several recently ing femalesof the recentlyestablished colonies establishedcolonies (Cape Direction, Cape Des- could be determined. However, although lacsand MontagueIsland). The remainingsev- breeding coloniesmay be genetically isolated en colonieswere all known or presumedto have through contemporaryphiloparry, patterns of predatedEuropean settlement. Philopatry may mtDNA differentiationmay be complicatedby be acting to maintain geneticdifferentiation be- the unstabledemographic history of this spe- tween breeding coloniesin this species,as has cies. been shown in colonially nesting Fairy Prions (Pachyptilaturtur) occupying a similar breeding range (Ovenden et al. 1991). If individual col- METHODS onies represent distinct intraspecific assem- We collected 335 shearwater chicks during the blages of mtDNA haplotypes, colony-specific southernsummer breeding seasonsfrom 1989to 1992 mtDNA markers could be used to identify the from 11 coloniesin southeasternAustralia (Fig. 1), 72 AUSTII•,W•ITE, ^I•I• OVEI•I•EI• [Auk,Vol. 111 T^BLE1. Numbers of 6/5.33-base restriction enzyme haplotypesscored from each of seven Short-tailed Shearwatercolonies. Each haplotype composed of morphdesignations for restrictionenzymes Aft II, Apa LI, Ava I, BanI, Bcl I, Bgl II, BstXI, EcoRV, Hae II, Hin dIII and Pvu II, respectively. Locality (n) i 3 2 4 5 6 11 Whale- Cape Cape Trial Little Great Mon- bone Deslacs Direc- Harbour Green Dog tague Point tion Island Island Island Haplotype (29) (29) (30) (30) (34) (39) (22) Total a AAAAAAAAAAA 14 19 17 17 23 25 13 128 b AAAAAAAABAA 6 5 6 5 4 7 4 37 c AAAAAAAACAA 2 1 2 4 1 2 i 13 d AABAAAAABAA 1 0 2 0 2 2 2 9 e AAAAAABAAAA 1 0 2 0 0 0 0 3 f AAAAABAABAA 0 0 0 i 0 1 0 2 g AAAACAAAAAA 0 1 0 0 I 0 0 2 h AAAAAAAADAA 2 0 0 0 0 0 0 2 i AABAAABAEAA i 0 0 0 0 0 0 1 j AAAADAAABAA i 0 0 0 0 0 0 1 k AAAAAADAAAA 1 0 0 0 0 0 0 1 I AAAAAAAAFAA 0 1 0 0 0 0 0 1 m AAAAAABABAA 0 1 0 0 0 0 0 1 n AAAAAACAAAA 0 i 0 0 0 0 0 1 o AABABAABBAA 0 0 i 0 0 0 0 1 p AAABAAAAAAA 0 0 0 1 0 0 0 1 q ABAAAAAAAAA 0 0 0 1 0 0 0 1 r BABAAAAABAA 0 0 0 i 0 0 0 1 s AAAAABAACAA 0 0 0 0 1 0 0 1 t AABABAAABAA 0 0 0 0 1 0 0 1 u BAAAAAAAAAA 0 0 0 0 i 0 0 1 v AABAAACABAA 0 0 0 0 0 1 0 1 w AAAAABAAAAA 0 0 0 0 0 1 0 1 x AAADAAAAAAA 0 0 0 0 0 0 1 1 y AABCAAAABAA 0 0 0 0 0 0 1 1 comprising: 6 colonies in Tasmania at Whalebone colonies and based on the results of the 6/5.33-base Point, Bruny Island (43ø28'S,147ø14'E, n = 29), Cape enzyme survey, the mtDNA of 231 individuals from Deslacs(42ø59'S, 147ø33'E, n = 30), Cape Direction WhalebonePoint, Trial Harbour, Great Dog Island, (43ø06'S, 147ø25'E, n = 30), Trial Harbour (41ø55'S, Port Fairy, Cape Woolamai, Doughboy Island, Gabo 145ø09'E,n = 30), Little Green Island (40ø13'S,148ø15'E, Island and Montague Island were analyzedwith four n = 35) and Great Dog Island (40ø15'S,148ø14'E, n = 4-baserestriction enzymes (Hha I, Hinf I, Msp I, Taq 39); 4 colonies in Victoria at Port Fairy (38ø24'S, I).
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