University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln
USGS Staff -- Published Research US Geological Survey
2011
Genetic Applications in Avian Conservation
Susan M. Haig U.S. Geological Survey, [email protected]
Whitcomb M. Bronaugh Oregon State University
Rachel S. Crowhurst Oregon State University
Jesse D'Elia U.S. Fish and Wildlife Service
Collin A. Eagles-Smith U.S. Geological Survey
See next page for additional authors
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Haig, Susan M.; Bronaugh, Whitcomb M.; Crowhurst, Rachel S.; D'Elia, Jesse; Eagles-Smith, Collin A.; Epps, Clinton W.; Knaus, Brian; Miller, Mark P.; Moses, Michael L.; Oyler-McCance, Sara; Robinson, W. Douglas; and Sidlauskas, Brian, "Genetic Applications in Avian Conservation" (2011). USGS Staff -- Published Research. 668. https://digitalcommons.unl.edu/usgsstaffpub/668
This Article is brought to you for free and open access by the US Geological Survey at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in USGS Staff -- Published Research by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Authors Susan M. Haig, Whitcomb M. Bronaugh, Rachel S. Crowhurst, Jesse D'Elia, Collin A. Eagles-Smith, Clinton W. Epps, Brian Knaus, Mark P. Miller, Michael L. Moses, Sara Oyler-McCance, W. Douglas Robinson, and Brian Sidlauskas
This article is available at DigitalCommons@University of Nebraska - Lincoln: https://digitalcommons.unl.edu/ usgsstaffpub/668 The Auk 128(2):205–229, 2011 The American Ornithologists’ Union, 2011. Printed in USA.
SPECIAL REVIEWS IN ORNITHOLOGY
GENETIC APPLICATIONS IN AVIAN CONSERVATION SUSAN M. HAIG,1,6 WHITCOMB M. BRONAUGH,2 RACHEL S. CROWHURST,2 JESSE D’ELIA,2,3 COLLIN A. EAGLES-SMITH,1 CLINTON W. EPPS,2 BRIAN KNAUS,4 MARK P. M ILLER,1 MICHAEL L. MOSES,2 SARA OYLER-MCCANCE,5 W. DOUGLAS ROBINSON,2 AND BRIAN SIDLAUSKAS2
1U.S. Geological Survey, Forest and Rangeland Ecosystem Science Center, 3200 SW Jefferson Way, Corvallis, Oregon 97331, USA; 2Department of Fisheries and Wildlife, Oregon State University, 104 Nash Hall, Corvallis, Oregon 97331, USA; 3U.S. Fish and Wildlife Service, Pacific Regional Office, 911 NE 11th Avenue, Portland, Oregon 97232, USA; 4U.S. Forest Service, Pacific Northwest Research Station, 3200 SW Jefferson Way, Corvallis, Oregon 97331, USA; and 5U.S. Geological Survey, Fort Collins Science Center, 2150 Centre Avenue, Building C, Fort Collins, Colorado 80526, USA
A fundamental need in conserving species and their hab- , Garnett and Christidis , Haig and D’Elia ). Despite itats is defining distinct entities that range from individuals to the importance of defining these units, boundaries of species, sub- species to ecosystems and beyond (Table ; Ryder , Moritz species, and populations are not always clear, and hybridization , Mayden and Wood , Haig and Avise , Hazevoet can further conflate taxonomic analyses and conservation options , Palumbi and Cipriano , Hebert et al. , Mace , (Haig and Allendorf ). Advances in conservation genetics Wheeler et al. , Armstrong and Ball , Baker , Ellis have proved helpful in resolving some long-standing taxonomic et al. , Winker and Haig ). Rapid progression in this inter- questions in birds, but philosophical disagreements over funda- disciplinary field continues at an exponential rate; thus, periodic mental taxonomic concepts remain. updates on theory, techniques, and applications are important for Species.—Although birds are arguably the best-studied informing practitioners and consumers of genetic information. vertebrate group, vigorous debate continues over which spe- Here, we outline conservation topics for which genetic informa- cies definition best applies to them. The three top contenders tion can be helpful, provide examples of where genetic techniques include the biological species concept (BSC; see Tobias et al. , have been used best in avian conservation, and point to current Winker a)—the most commonly used in avian taxonomy— technical bottlenecks that prevent better use of genomics to re- and two that have emerged from cladistics (the phylogenetic and solve conservation issues related to birds. We hope this review will monophyletic species concepts; Cracraft , ; Mishler and provide geneticists and avian ecologists with a mutually beneficial Brandon ; McKitrick and Zink ; Zink and McKitrick dialogue on how this integrated field can solve current and future ). In part because of the multiplicity of applied species con- problems. cepts, avian taxonomy is far from stable at any level, and this has real-world conservation implications. For example, patterns TAXONOMY of endemism in the birds of Mexico (Peterson and Navarro- Sigüenza ) and the Philippines (Peterson ) depend on If conservation strives to preserve as much variation as possible whether a biological or phylogenetic species concept is used. The at all levels of biodiversity, then conservation depends upon tax- use of different species concepts has also been shown to affect onomy. Whether conservation priorities are based on species, the composition of lists of endangered birds in Mexico (Rojas- subspecies, or evolutionarily significant units (ESUs), DNA is Soto et al. ), and vigorous discussion regarding the appro- increasingly being used to determine the evolutionary and geo- priateness of splitting polytypic species continues (Christidis graphic boundaries of these entities. Far from merely academic and Boles , Chesser et al. ). At the same time, new dia- considerations, these groupings are critically important in con- logues are emerging about the importance of studying specia- servation prioritization and can have important legal ramifica- tion patterns in migratory birds, given that differentiation and tions for threatened and endangered species, subspecies, distinct speciation appear to be common even in the absence of extended population segments (DPSs), or ESUs (reviewed in Haig et al. isolation (Winker b).
6Secondary authorship is alphabetical. E-mail: [email protected]
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TABLE 1. Issues addressed by avian conservation genetics.
Taxonomy (Meta) populations Landscapes s 7HAT ARE THE EVOLUTIONARY AND s 7HAT ARE LEVELS OF GENETIC DIVERSITY s 7HAT ARE THE EFFECTS OF LANDSCAPE FEATURES AND GEOGRAPHIC BOUNDARIES OF SPECIES POPULATION STRUCTURE EFFECTIVE LANDSCAPE HETEROGENEITY ON GENETIC DIVERSITY SUBSPECIES AND MANAGEMENT UNITS POPULATION SIZE OR GENE mOW AND AND POPULATION STRUCTURE s 7HAT IS THE EXTENT OF INTROGRESSION OR HOW HAVE THEY CHANGED OVER TIME s (OW ARE PHYLOGEOGRAPHIC PATTERNS OF BIRDS HYBRIDIZATION s 7HAT IS THE BEST STRATEGY FOR MANAGING CHANGING IN RESPONSE TO CLIMATE CHANGE s 7HICH SPECIES ARE REPRESENTED IN SMALL POPULATIONS TO MAXIMIZE s 7HICH POPULATIONS OR LIFE STAGES ARE MOST ILLEGAL WILDLIFE TRADE CONSERVATION OF GENETIC DIVERSITY AFFECTED BY CONTAMINANT EXPOSURE ARE CERTAIN s 7HAT CRYPTIC SPECIES HAVE BEEN PEDIGREE ANALYSES GENOTYPES MORE VULNERABLE MISCLASSIlED s 7HAT IS THE EXTENT OF POPULATION s )N MIXED STOCK POPULATIONS WHAT PROPORTION s (OW IS BIODIVERSITY CHANGING IN CONNECTIVITY OR ISOLATION OF EACH STOCK IS BEING HARVESTED OR AFFECTED BY RESPONSE TO CLIMATE CHANGE s 7HICH POPULATIONS WOULD BE THE ENVIRONMENTAL PERTURBATIONS s 7HAT IS THE IDENTITY OF A HYBRID BEST SOURCE FOR A TRANSLOCATION OR CRYPTIC SPECIMEN OR THE REMAINS REINTRODUCTION OF AN ANCIENT OR RECENT SPECIMEN s (OW DO INDIVIDUALS AND POPULATIONS s 7HAT IS THE BEST AVIAN TREE OF LIFE FOR MOVE THROUGHOUT THE ANNUAL CYCLE PRIORITIZING BIODIVERSITY CONSERVATION s (OW ARE DISEASE TRANSMISSION BY PHYLOGENETIC DIVERSITY PATHWAYS LINKED TO BIRD MOVEMENTS
While debate over species concepts endures, the increasing four potential cryptic species, one within the White-breasted ease and affordability of DNA sequence analysis provides new Tapaculo (E. indigoticus) and three within the Mouse-colored power for discriminating among morphologically similar taxa, Tapaculo (S. speluncae). and continues to change our understanding of avian taxonomy Once putative cryptic species are identified with genet- (insets and ; Bickford et al. ). Nearly all easily recognized ics, analyses of song and closer inspection of morphology often bird species were thought to be described decades or centuries provide additional support for the species status. However, spe- ago, leading ornithologists to conclude by the s that there cies will not always diverge equally in all character systems, as were few undiscovered bird species or geographic races (Zimmer demonstrated by recent studies of warbler finches (Certhidea) and Mayr , Stresemann ). However, continued discovery in the Galápagos. These morphologically conservative birds are of new avian taxa into the st century indicates that conclusion the most basal and widespread of Darwin’s finches and do not to have been premature. Just within the antbirds (Thamnophili- exhibit any premating isolation due to song, so they have tradi- dae), the American Ornithologists’ Union (AOU) has recognized tionally been treated as one species (Grant and Grant ). Re- an additional species since and elevated subspecies to cent discovery of large intraspecific genetic differences resulted full species status while lumping just two species together (Remsen in recognition of two species (C. olivacea and C. fusca; Freeland et al. ). and Boag , Petren et al. ). These genetic differences Genetic analyses have been critical to most recent discov- were not correlated with geography, as in most cases of cryptic eries of new birds because these are usually cryptic species with diversity, but were instead associated with habitat differences subtle or indistinguishable external characters resulting from (Tonnis et al. ). evolutionarily conservative morphology, a reliance on nonvisual Many have pointed out that using multiple lines of evidence mating cues, or convergent morphological evolution (Bickford (DNA, song, morphology, ecology, etc.) in taxonomic decisions et al. , Trontelj and Fišer ). In the case of the Gray-crowned may lead to incongruent results (Zink , O’Brien and Mayr Palm-Tanager (Phaenicophilus poliocephalus), Sly et al.’s () , Ball and Avise , Zink ), leading some to advocate identification of two taxa, with one being Haiti’s only endemic use of mitochondrial DNA (mtDNA) over other data in making bird, led to renewed interest in protecting a threatened biodi- such delineations (Ball and Avise , Zink et al. , Zink versity hotspot on the Tiburon Peninsula. Studies of tapaculos ). Others have emphasized the need for multilocus data in the genus Scytalopus (Rhinocryptidae) also demonstrate the (Edwards and Beerli ) and more inclusive approaches that ability of genetic data to reveal unrecognized biodiversity. These combine genetic data with data from plumage, morphology, small mouse-like birds of the Andes and southeastern Brazil song, and behavior (Dizon et al. , Vogler and DeSalle , inhabit the dark undergrowth of forests and scrub. Scytalopus Haig et al. , Alström et al. ). Tobias et al. () took song has often been used to define species’ limits because their this a step further and proposed using a scoring system based morphology is so static over evolutionary time that they often on biometrics, plumage, and song to measure divergence be- vary more within than among species (Krabbe and Schulenberg tween undisputed sympatric species as a yardstick for assess- ). Thus, it was quite surprising when Maurício et al. () ing the taxonomic status of allopatric forms. Although it needs tested Scyatlopus monophyly with molecular data and discov- further testing, their approach yielded relatively few changes to ered a cryptic genus, Eleoscytalopus. Subsequently, Mata et al. avian taxonomy in Europe. They argued that the benefits of this () used mitochondrial and nuclear DNA sequences to reveal approach include a systematic and defensible approach that can APRIL 2011 — SPECIAL REVIEWS IN ORNITHOLOGY — 207
HIGH-THROUGHPUT SEQUENCING AND SINGLE-NUCLEOTIDE POLYMORPHISMS
(IGH THROUGHPUT SEQUENCING TECHNOLOGY OFFERS THE CAPACITY TO QUICKLY COLLECT A TREMENDOUS AMOUNT OF GENETIC DATA FROM SELECT INDIVIDUALS (UDSON AND HAS CREATED A NEW GOLD STANDARD FOR MULTILOCUS DATA SETS THAT SAMPLE ACROSS MANY UNLINKED PORTIONS OF THE GENOME -ARDIS ,ERNER AND &LEISCHER 4HE ANALYTICAL POWER AFFORDED BY LARGE GENETIC DATA SETS IS REVOLUTIONIZING GENOMIC STUDIES OF BIRDS AT EV ERY SPATIAL AND TEMPORAL SCALE %DWARDS ET AL (ACKETT ET AL *ENNINGS ET AL 7HERE PREVIOUS AVIAN POPULATION OR PHYLOGEO GRAPHIC STUDIES MIGHT EMPLOY TO VARIABLE MICROSATELLITE LOCI AT BEST NOW HUNDREDS OF THOUSANDS OF VARIABLE LOCI ARE EASILY ATTAINABLE AND AT FAR LOWER COSTS IN SUPPLIES AND PERSONNEL -OLECULAR MARKERS USED IN TRADITIONAL STUDIES WERE THOUGHT TO BE SELECTIVELY NEUTRAL AND SAMPLED ONLY A MINUTE PORTION OF THE GENOME PARTICULARLY IN AVIAN STUDIES ! LIMITATION OF SUCH STUDIES HOWEVER LIES IN THEIR ASSUMPTIONS THAT THE DETECTED LEVEL OF NEUTRAL GENETIC VARIATION IN A POPULATION IS CORRELATED WITH LEVELS OF FUNCTIONALLY IMPORTANT VARIATION AND THAT LOW LEVELS OF FUNCTIONAL VARIATION LEAD TO LOW lTNESS AND LOW ABILITY TO ADAPT TO FUTURE CHANGE (IGH THROUGHPUT SEQUENCING AND OTHER ADVANCES IN GENOMICS ALLOW FOR NOT ONLY THE EXPANSION OF THE AMOUNT OF THE GENOME EXAMINED BUT ALSO THE DETECTION AND CHARACTERIZATION OF FUNCTIONAL GENES THAT ARE RESPONSIBLE FOR SURVIVAL AND ADAPTATION 4HIS NEW ABILITY TO SCAN THE ENTIRE GENOME FOR VARIATION IS EXTREMELY USEFUL IN GENOMIC STUDIES AS IN CASES WHERE NOMINAL SUBSPECIES OF BIRDS DIFFER GREATLY IN MORPHOLOGY SONG OR BEHAVIOR BUT NOT IN THE SE QUENCE OF COMMONLY USED MOLECULAR MARKERS SUCH AS CYTOCHROME b or CYTOCHROME OXIDASE ) :INK )N SOME CASES GENOME WIDE SCANS MAY HELP PICK OUT FAST EVOLVING LOCI THAT CONTRIBUTE TO THE OBSERVED PHE NOTYPIC DIFFERENCES FOR A CELEBRATED EXAMPLE IN MICE SEE (OEKSTRA ET AL THEREBY RECONCILING APPARENT CONmICT BETWEEN MOLECULES AND MORPHOLOGY #ONVERSELY THE SUCCESS OF MANY RECENT STUDIES IN EMPLOYING A CON CISE SET OF MITOCHONDRIAL AND NUCLEAR MARKERS TO DELINEATE SPECIES AND SUBSPECIES "ARROWCLOUGH ET AL /YLER -C#ANCE ET AL B 0ETERS ET AL "ARKER ET AL 2OSS ET AL AND THE MULTI PLICITY OF AVAILABLE METHODS FOR SPECIES DELIMITATION 3ITES AND -ARSHALL 7IENS DEMONSTRATE THAT SOLID TAXONOMIC CONCLUSIONS CAN BE DRAWN FROM SMALL FRACTIONS OF THE GENOME )N THAT LIGHT TRADITIONAL 3ANGER SEQUENCING OF MANY INDIVIDUALS FOR RELATIVELY FEW CAREFULLY CHO SEN LOCI MAY CONTINUE TO PRESENT A COST EFFECTIVE APPROACH TO PROBLEMS IN TAXONOMY FOR MANY YEARS TO COME (OWEVER NEXT GENERATION HIGH THROUGHPUT SEQUENCING REPRESENTS AN IMPORTANT NEW ADDITION TO THE conservation genetic toolbox. 0ERHAPS THE NEWEST ASPECT OF UTILIZING HIGH THROUGHPUT SEQUENCING FOR AVIAN CONSERVATION GENETICISTS IS THE USE OF SINGLE NUCLEOTIDE POLYMOR PHISMS 3.0S &IG 3.0S ARE THE MOST ABUNDANT TYPE OF GENETIC POLY MORPHISM IN ANY GENOME AND THOSE FOUND WITHIN A CODING SEQUENCE ARE OF PARTICULAR INTEREST BECAUSE THEY ARE MORE LIKELY TO ALTER THE BIOLOGI CAL FUNCTION OF A PROTEIN !LTHOUGH AN INDIVIDUAL 3.0 HAS LIMITED POLY MORPHISM THERE ARE ONLY FOUR STATES GIVEN THE TWO NUCELEOTIDES USE OF HIGH THROUGHPUT SEQUENCING PROVIDES EASY ACCESS TO THE DEVELOPMENT OF HUNDREDS OF 3.0S FOR A PARTICULAR STUDY 4HUS THEY ARE INCREASINGLY BE ING USED AS MARKERS IN NATURAL POPULATION STUDIES BECAUSE THEY PROVIDE AN OPPORTUNITY TO ASSESS A LARGE NUMBER OF UNLINKED LOCI FOR A RANGE OF FIG ! SINGLE NUCLEOTIDE POLYMORPHISM 3.0 IS A $.! SE QUESTIONS 3LATE ET AL (OWEVER 3.0 USE IN AVIAN STUDIES IS JUST BE QUENCE VARIATION THAT OCCURS WHEN A SINGLE NUCLEOTIDE DIFFERS GINNING THEIR DISTRIBUTION LINKAGE MAPPING AND SO ON HAVE BEEN INVES BETWEEN MEMBERS OF A SPECIES OR PAIRED CHROMOSOMES IN AN IN TIGATED ONLY RECENTLY "ACKSTRÚM ET AL +IMBALL ET AL DIVIDUAL 4HUS IT IS A CHANGE OF A NUCLEOTIDE AT A SINGLE BASE PAIR 0RECIOUS FEW AVIAN CONSERVATION STUDIES HAVE USED 3.0S THUS FAR 'ARCÓA LOCATION ON $.! )N THE EXAMPLE SHOWN HERE TWO SEQUENCED AND !RRUGA USED 3.0S TO DIFFERENTIATE SPECIES OF PARTRIDGES FOR RE INTRODUCTION AND 6ËLI ET AL USED THEM TO EXAMINE HYBRIDIZATION $.! FRAGMENTS FROM DIFFERENT INDIVIDUALS CONTAIN A DIFFERENCE BETWEEN TWO SPECIES OF SPOTTED EAGLES IN %UROPE #LEARLY THE FUTURE IS in a single nucleotide (AAGCCTA to AAGCTTA 4HEREFORE UPON US GIVEN THE POWER OF HIGH THROUGHPUT SEQUENCING AND THE ASSOCI THERE ARE TWO ALLELES C and T -OST 3.0S HAVE ONLY TWO ALLELES ATED POWER UTILITY OF 3.0S &IGURE BY $ (ALL
be applied across taxa worldwide. This sort of methodology, ex- Thus, one may capture variation due to multiple influences on panded to include genetic data, could benefit conservation by speciation and move toward a taxonomy that best reflects likely providing a consistent approach that includes multiple lines of separations among gene pools, even when it is not possible to taxonomic evidence by combining neutral genetic markers with demonstrate strict reproductive isolation. phenotypic data that likely reflect the influence of reproduc- Two recent investigations exemplify the use of multiple tive isolation (Haig et al. , Garnett and Christidis ). lines of evidence to assess taxonomic boundaries: studies of the 208 — SPECIAL REVIEWS IN ORNITHOLOGY — AUK,VOL. 128
BARCODING
$.! BARCODING IS A POWERFUL GENETIC TOOL THAT SEEKS TO SEQUENCE SPECIlC SHORT PORTIONS OF THE GENOME IN ANIMALS TYPICALLY CYTOCHROME OXIDASE ) ;#/)= OF ALL ORGANISMS ON THE PLANET TO AID IN SPECIES IDENTIlCATION &IG (EBERT ET AL -ORITZ AND #ICERO (EBERT AND 'REGORY 2ATNASINGHAM AND (EBERT "AKER ET AL "ARCODES PROMISE AN EASY WAY TO RELIABLY DETERMINE SPECIES MEMBERSHIP EVEN IN CASES WHERE MORPHOLOGY BASED IDENTIlCATION IS DIFlCULT AS IN THE CASE OF JUVENILES ISOLATED FEATHERS OR THE REMAINS OF BIRDS UNLUCKY ENOUGH TO BE SUCKED INTO JET ENGINES !S SEQUENCING BECOMES LESS EXPENSIVE AND EASIER TO PERFORM BARCODES ALSO OFFER A POWERFUL WAY FOR NON EXPERTS CITIZEN SCIENTISTS AND PEOPLE IN THE DEVELOPING WORLD TO CONDUCT BIODIVERSITY SURVEYS "ARCODING HAS ATTRACTED MAJOR FUNDING OVER THE PAST DECADE SEE EG www.dnabarcoding.ca/ AND THE CORRESPONDING RISE OF INI TIATIVES SUCH AS THE "ARCODE OF ,IFE PROJECT WWWBARCODEOmIFEORg SPARKED DEBATE IN TAXONOMIC CIRCLES OVER THE RELATIVE MERIT OF MO LECULAR AND MORPHOLOGICAL APPROACHES TO TAXONOMY 4AUTZ ET AL (EBERT ET AL 7HEELER ET AL 7ILL AND 2UBINOFF $E3ALLE ET AL (EBERT AND 'REGORY (AJIBABAEI ET AL )N THE FACE OF MAJOR CRITICISM THAT THE INFORMATION CONTAINED IN A SINGLE GENE COULD NOT BE USED TO RELIABLY RECONSTRUCT PHYLOGENY OR DELIMIT SPECIES 7ILL ET AL "ROWER 2UBINOFF BE CAUSE OF INTROGRESSION INSUFlCIENT SIGNAL INCOMPLETE LINEAGE SORTING AND VARIOUS OTHER PROBLEMS ADVOCATES OF BARCODING POINTED OUT THAT BARCODES COULD STILL YIELD REMARKABLY RELIABLE IDENTIlCATIONS FOR KNOWN SPECIES AS IN A PIONEERING STUDY OF BIRDS THAT FOUND THAT #/) SEQUENCE VARIATION AMONG SPECIES TYPICALLY EXCEEDED VARIATION WITHIN SPECIES BY FOLD (EBERT ET AL ! LATER MORE COMPREHEN SIVE STUDY +ERR ET AL REVEALED INSTANCES IN WHICH #/) FAILED TO PROVIDE SUFlCIENT INFORMATION TO IDENTIFY ALL BIRD SPECIES TESTED BUT EVEN SO THE SUCCESS RATE WAS WITH DIFlCULTIES BEING MOSTLY CONlNED TO CLUSTERS OF RECENTLY DIVERGED SPECIES OR CASES OF POSSIBLE HYBRIDIZATION ! SIMILAR STUDY FOUND THAT SINGLE LOCUS BARCODES CAN IDENTIFY AND OF KNOWN MARINE AND FRESHWATER lSHES RE SPECTIVELY 7ARD ET AL %VEN MOST PAIRS OF SISTER SPECIES CAN BE RELIABLY SEPARATED BY #/) BARCODES (EBERT ET AL 4AVARES AND "AKER /N THE BASIS OF THOSE SUCCESSES BROAD UTILITY OF THE APPROACH FOR ASSIGNING UNKNOWN INDIVIDUALS TO KNOWN SPECIES IS NOW ACCEPTED BY MANY BUT THERE ARE STILL IMPORTANT CAVEATS 4HE BARCODING APPROACH RELIES ON THE EXISTENCE OF A COMPREHENSIVE REFERENCE DATABASE %KREM ET AL AND SUCH DATABASES CAN BE MISLED BY THE PRESENCE OF NUCLEAR MITOCHONDRIAL PSEUDOGENES 3ONG ET AL &URTHERMORE MULTIPLE BARCODE LOCI MAY BE RE QUIRED FOR RELIABLE IDENTIlCATION IN CERTAIN TAXA #"/, 0LANT 7ORK ING 'ROUP +RESS ET AL THE BARCODE METHOD STILL FAILS to discriminate a small but important percentage (a OF KNOWN FIG SPECIES IN EVEN WELL STUDIED GROUPS -EYER AND 0AULAY +ERR #OLOR CODED BARCODES FOR THE "LACK 4ERN Chlidonias niger ET AL 7ARD ET AL AND THE RELIABILITY OF BARCODE BASED TOP AND THE 7HITE WINGED 4ERN C. leucopterus BOTTOM ILLUSTRATE IDENTIlCATION DECLINES PRECIPITOUSLY IN GROUPS THAT LACK A WELL STUD THE EASE WITH WHICH SPECIES CAN BE QUICKLY IDENTIlED AND DIFFEREN IED TAXONOMY -EYER AND 0AULAY TIATED )MAGE PREPARED BY +EVIN +ERR 53 .ATIONAL -USEUM &OR ALL ITS STRENGTHS BARCODING IS BEST SEEN AS AN ENHANCEMENT TO AND NOT AS A REPLACEMENT FOR CONVENTIONAL TAXONOMIC INVESTIGATIONS !LTHOUGH BARCODE APPROACHES CAN RECOGNIZE WHETHER A TEST SEQUENCE DOES OR DOES NOT CLOSELY MATCH THOSE ALREADY IN THE DATABASE AND THUS SUGGEST THE PRESENCE OF A POTENTIAL NEW SPECIES IN THE LATTER CASE RELI ANCE ON BARCODE DATA ALONE CAN OVERLOOK SPECIES (ICKERSON ET AL "ROWER AND SPECIES DELIMITATION IS BEST ACCOMPLISHED WITH MULTIPLE GENES AND MULTIPLE LINES OF EVIDENCE -ORITZ AND #ICERO 7ILL ET AL &OR EXAMPLE IN A RECENT COMPREHENSIVE DEFENSE OF SINGLE LOCUS BARCODING "AKER ET AL EXPLICITLY STATED THAT hMORE RIGOROUS METHODS OF SPECIES DELIMITATION SHOULD BE FAVORED USING COALESCENT BASED TECHNIQUES THAT INCLUDE TESTS OF CHANCE RECIPROCAL MONOPHYLY AND TIMES OF LINEAGE SEPARATION AND SEQUENCE DIVERGENCEv 4HEIR STATEMENT IS FAR FROM AN INDICTMENT OF BARCODE BASED APPROACHES TO IDENTIlCATION IT SIMPLY ACKNOWLEDGES THAT THE DATABASE UNDERLYING BARCODE IDENTIlCATIONS SHOULD BE BASED ON THE MOST RIGOROUS TAXONOMY AND SPECIES DELIMITATION POSSIBLE AND THAT BARCODING CAN ENHANCE BUT SHOULD NEVER REPLACE THE MANY CONTRIBUTIONS OF TRAINED SYSTEMATISTS
Spotted Bush-Warbler (Bradypterus thoracicus) complex by Recent splitting of Greater Sage-Grouse (C. urophasianus) Alström et al. () and studies of the Stripe-headed Brush- into two species (now including Gunnison Sage-Grouse [C. mini- Finch (Arremon torquatus) complex by Cadena and Cuervo (). mus]; Young et al. ) illustrates how recognition of cryptic spe- The former compared plumage, morphology, egg coloration, song, cies can carry major conservation implications (Hazevoet ). mtDNA haplotypes, habitat–altitudinal distribution, and behav- The Gunnison Sage-Grouse comprises less than , individu- ior and suggested that B. thoracicus, B. davidi, and B. kashmirensis als, and threats are considered imminent and of high magnitude, should be recognized as full species because they differ in most whereas the population of Greater Sage-Grouse, although sig- aspects. Similarly, Cadena and Cuervo () used data from song, nificantly reduced from historical numbers, is still estimated to morphology, ecology, and genetics to suggest recognition of eight exceed , individuals, and threats to this species are con- full species in a group formerly treated as a conglomerate of sidered moderate in magnitude (U.S. Fish and Wildlife Service subspecies. [USFWS] a, b). Although both species are now considered APRIL 2011 — SPECIAL REVIEWS IN ORNITHOLOGY — 209
candidates under the U.S. Endangered Species Act (ESA; i.e., they basis for adaptation and phenotypic variation may help sort out were found to warrant ESA protection but listing is currently pre- the issue (Hoekstra et al. , Mumme et al. , Mitchell- cluded by higher-priority listing actions), the Gunnison Sage- Olds et al. ). Grouse has a higher listing priority than the Greater Sage-Grouse, Decisions to recognize or not recognize subspecies have which means that it is likely to receive ESA protection sooner than significant conservation implications under many endangered- the Greater Sage-Grouse, and sooner than it would have if it were species classification and funding schemes (reviewed in Haig et al. listed as a subspecies or DPS. It is also possible, given the higher , Haig and D’Elia ). For example, there would be no tax- level of threats and smaller population size, that the Gunnison onomic units below the species level if the phylogenetic species Sage-Grouse could ultimately receive a higher level of protection concept (PSC) were adopted by the AOU. Thus, USFWS, IUCN, under the ESA than the Greater Sage-Grouse. COSEWIC (Committee on the Status of Endangered Wildlife in Subspecies.—While the goal of species conservation is shared Canada), and others would have to reconsider current avian sub- by all who value biodiversity, the existence, identification, and species listings. In the United States, subspecies would have to conservation of subspecies has received mixed support (Zink be re-examined for listing as either species or some other entity , Haig et al. , Haig and D’Elia , Winker and Haig such as a DPS or ESU. Elevation of subspecies to species (under the ). A “subspecies” is generally defined as a breeding population PSC) could aid conservation efforts because such entities could that has measurably distinguishable genotypes or phenotypes (or be given added weight corresponding to their elevated taxonomic both) and occupies a distinct geographic area within its species status under the IUCN criteria. However, many other difficul- range (Mayr , Avise , Patten , Remsen ). Vari- ties could result. For one, the change could make it more difficult ation below the species level can embody evolutionary and de- to add species to various endangered-species lists because of the velopmental responses to heterogeneous geography, differential added workload, cost, and, perhaps, public fatigue from hearing selection, or neutral processes such as bottlenecks and stochas- about many new species being listed simply because a new species ticity. Some of the strongest arguments about the validity of the concept has been applied. Furthermore, it could reopen litigation subspecies concept describe attempts to delineate its upper and regarding the listings. Swamping the IUCN list with many new lower bounds (Winker a). That is, at what point is geographic “species” could reduce the importance of a former “species” with a variation suitably differentiated to justify subspecific status and at wider geographic range. Finally, adopting the PSC and recogniz- what level of differentiation do recognized subspecies achieve full ing many more avian species could exacerbate the difficulty of vi- species status? sual identification or differentiation of species by law-enforcement Although ornithologists have traditionally defined avian agents around the world who often struggle to identify particular subspecies (and species) using plumage, morphology, and behav- species under even the BSC criteria. Overall, the changes to pol- ior, advances in molecular biology have led to the use of variation icy that would arise from adopting the PSC argue neither for nor in discrete and presumably selectively neutral genetic markers against the biological validity of that concept, but effectively illus- (Winker and Haig ). These molecular data provide an addi- trate that the species-concept debate carries major implications tional avenue for taxon delineation, but in many cases the mo- for conservation. lecular data sets are not congruent with subspecies defined by Hybridization.—Hybridization and introgression can result in traditional methods (Zink , ; O’Brien and Mayr ; extinction of native fauna when nonindigenous species are intro- Ball and Avise ; Burbrink et al. ; Funk et al. b; duced or disperse into novel environments (Rhymer and Simberloff Draheim et al. ; Zink et al. ). Zink () argued that , McCarthy , Mallet ). Molecular methods are the subspecies defined by traditional nonmolecular methods may fastest and most accurate means of revealing boundaries between actually misinform conservation efforts through misrepresenta- known taxonomic entities that are permeable or under erosion, tion of underlying patterns of intraspecific variation. This lack as in the case of hybridization. Allendorf et al. () developed of concordance among approaches has led some to suggest that hybrid categorization guidelines to assist with management deci- molecular methods (i.e., reciprocal monophyly among mito- sions. These are particularly useful for those species that receive chondrial sequences) should be used preferentially to define con- protection under the ESA and where law-enforcement agents need servation units (Moritz , Zink ). Others suggest that to accurately identify taxa to decide whether or not a violation of discordance should be expected when using neutral molecular the ESA’s prohibited acts (ESA section ) has occurred. Hybrids are data to examine shallow levels of divergence, as compared with not protected under the ESA, IUCN, or SARA (Species at Risk Act), phenotypic data sets that describe variation that is likely reflec- which has caused numerous debates, especially for species listed tive of processes that are not selectively neutral (Greenberg et under the ESA (for review, see Haig and Allendorf ). Problems al. , Oyler-McCance et al. , Pruett and Winker , arise when a listed species hybridizes with a nonlisted species and Winker a). the hybrids are not visually distinguishable from the listed taxa, At present, so few described avian subspecies have received leaving law-enforcement agents unable to prosecute a person who examination via modern molecular methods that it is difficult has harmed or killed the listed species, unless they have access to to draw general conclusions about the validity or utility of the molecular tools that can sort hybrids from listed species. subspecies concept (but see Klicka et al. ). Thus, new, ge- Owls in genus Strix exemplify the utility of genetic tools in netically informed attention to intraspecific variation across a resolving conservation issues complicated by hybridization. Hy- greater taxonomic range is warranted (Haig and Winker , bridization between threatened Northern Spotted Owls (Strix Remsen ). As the application of genomic methods become occidentalis caurina) and invasive Barred Owls (S. varia) occurs more widespread among avian taxa, examination of the genetic and viable offspring are produced (Hamer et al. , Kelly and 210 — SPECIAL REVIEWS IN ORNITHOLOGY — AUK,VOL. 128
Forsman ). However, Strix hybrids that backcross with Spot- greatly affect phylogenetic diversity measures when they result ted Owls produce fewer offspring, which potentially reduces their in long branches associated with higher taxa with few extant fitness (Haig et al. , Kelly and Forsman ). Mitochondrial species, or even species that form monotypic families or genera. DNA and amplified fragment length polymorphism (AFLP) anal- For example, in the New World, recent molecular studies have yses have proved to be reliable methods for accurate identifica- resulted in the erection or resurrection of monotypic families tion of Strix hybrids (Haig et al. ). Additionally, Funk et al. for the Osprey (Pandionidae: Pandion haliaetus), Magellanic (a) identified four diagnostic microsatellite loci that suc- Plover (Pluvianellidae: Pluvianellus socialis), Sharpbill (Oxy- cessfully differentiated F hybrids from backcrosses where AFLP runcidae: Oxyruncus cristatus), and Black-capped Donacobius and field identification methods failed. These markers are use- (Donacobiidae: Donacobius atricapilla) (Remsen et al. ). Di- ful to law-enforcement officials who must be able to discern be- versity in the order Ciconiiformes has been reduced from to tween “take” of Spotted Owls and hybrids to effectively protect species with the transfer of Ardeidae, Scopidae, Balaenicipiti- the Spotted Owl. dae, and Threskiornithidae to the Pelecaniformes (Chesser et al. Genetic markers may also be useful in identifying site- ). Similarly, phylogenetic analysis of molecular data sets of specific management actions for removing hybrids. Hawaiian New Zealand “honeyeaters” showed that the rare Stitchbird (No- Ducks (Anas wyvilliana), or Koloa, are a Federal and State en- tiomystis cincta), extirpated from North Island and numbering dangered species endemic to the Hawaiian islands and readily fewer than , individuals on an offshore island, represents a hybridize with introduced feral Mallards (A. platyrhynchos) monotypic family (Notiomystidae) with a divergence of mil- (Fowler et al. ). Fowler et al. () used AFLPs and micro- lion years ago (Ma) from its closest relatives, the New Zealand satellites to distinguish between hybrids and Hawaiian Ducks Wattlebirds (Callaeidae; Driskell et al. ). The Hawaiian Hon- and then to evaluate the relative contributions of Mallards and eycreepers (Mohoidae) are a similar case: all four species were Hawaiian Ducks to the hybrids. They found differences in the lost before they were identified to science (Fleischer et al. ). If contribution of hybrids on different islands, suggesting that a goal of conservation is to preserve as much of the tree of life as island-specific management actions may be warranted. Finally, possible, consideration should be given to protecting regions that because they were able to effectively differentiate hybrids and harbor these highly divergent taxa. Molecular data can often pro- Hawaiian Ducks using molecular tools, a morphological field vide a clear window into the true structure of that tree. key is being created and tested with molecular data to help guide hybrid-removal actions. POPULATION STRUCTURE Levels of hybridization and introgression of the critically en- dangered New Zealand Black Stilt or Kaki (Himantopus novaeze- Development of microsatellite markers in the s revolution- landiae) with the self-introduced congener, the Pied Stilt or Poaka ized our ability to understand population structure in birds. New (H. himantopus leucocephalus), were documented using a Bayes- sequencing technology has exponentially increased this capabil- ian admixture analysis of microsatellite data with mitochondrial ity (inset ; Lerner and Fleischer ). Further, comparing mi- DNA sequence data (Steeves et al. ). From this analysis it was crosatellite results with mitochondrial sequence data juxtaposes demonstrated that hybrids could be identified by plumage charac- recent population processes with changes in population structure teristics and that, despite extensive and bidirectional hybridiza- over evolutionary time. Thus, detailed estimates of genetic diver- tion, there was almost no evidence for introgression from Poaka to sity, population structure, effective population size, and gene flow Kaki, which is likely attributable to reduced reproductive success are now possible and robust where previously such estimates were in female hybrids and a transient male-biased Kaki sex ratio. Such problematic in bird studies. a finding was counter to popular beliefs and critical to deciding Consideration of demographic information with genetic data whether or not to promote hybridization to facilitate genetic res- further strengthens our understanding of detailed population cue, or whether to prevent it. structure. Funk et al. () used this approach to identify recent Conservation prioritization.—Even after taxa are delineated, population bottlenecks for Northern Spotted Owls (Strix occi- limited resources force biologists, managers, and policymakers to dentalis caurina) and found that genetic results were correlated implement triage when allocating funds for conservation (Bottrill with long-term demographic trends from the same sites. A severe et al. ). Various taxonomy-based prioritization schemes have ancient bottleneck was also detected in the British Golden Eagle been proposed. For example, phylogenetic diversity measures (Aquila chrysaetos), although in this case the bottleneck did not may be used to prioritize biodiversity conservation based on evo- appear to affect demographic stability (Bourke et al. ). Con- lutionary history, thereby affording increased protection to dis- versely, Brekke et al. () found severe inbreeding depression tinctive taxa (Vane-Wright et al. , Faith ) at any level of among a reintroduced population of the endangered Hihi (Notio- taxonomic hierarchy (Avise ). Phylogenetic approaches to mystis cincta) in New Zealand. conservation are flexible and powerful, but they are dependent on Integration of ancient DNA (inset ) into analyses of popula- phylogenetic hypotheses that are themselves works in progress tion structure can provide a more direct view of historical popu- and can sometimes change considerably when new data or meth- lation structure and identify otherwise cryptic phylogeographic ods of analysis become available. For example, the last three an- patterns. For example, using ancient mtDNA from bones pre- nual supplements to the AOU Check-list of North American Birds served in lava tube caves, Paxinos et al. () found a previously (Banks et al. ; Chesser et al. , ) added four orders unknown radiation of geese in the Hawaiian archipelago associ- and families to the previous list as a direct result of new stud- ated with the independent evolution of flightlessness and gigan- ies on the avian tree of life (Hackett et al. ). Such changes tism on different islands. APRIL 2011 — SPECIAL REVIEWS IN ORNITHOLOGY — 211
ANCIENT DNA
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CAN BE INSUFlCIENT TO ACCURATELY INFER POPULATION HISTORIES BECAUSE RECONSTRUCTIONS FROM MODERN DATA RELY ON EXTRAPOLATIONS RATHER THAN DIRECT OBSERVATIONS OF THE FOSSIL RECORD 7AYNE ET AL 4HIS RENDERS THEM BIASED TOWARD REmECTING RECENT OR EXTREME EVENTS EG RECENT POPULATION BOTTLENECKS 'ROOMBRIDGE ET AL 2AMAKRISHNAN AND (ADLY 0EERY ET AL 4HUS CAUTION IS WARRANTED WHEN INTERPRETING RESULTS FROM A$.! STUDIES THAT RELY ON SPECIMENS FROM A SINGLE PERIOD )NCLUSION OF A$.! ACROSS MULTIPLE PERIODS MAY IMPROVE THE RELIABILITY OF HISTORICAL POPULATION RECONSTRUCTIONS 2AMAKRISHNAN AND (ADLY 212 — SPECIAL REVIEWS IN ORNITHOLOGY — AUK,VOL. 128
Comparing results across taxa can also help illuminate small translocations, or predict potential changes in effective popula- population processes. Evans and Sheldon () analyzed micro- tion size as a result of better pedigree or population management satellite data from bird species and found a significant decline (Haig and Ballou ). Recently, pedigree analyses have proved in mean heterozygosity with increasing extinction risk. They sug- helpful in developing management plans for maintaining genetic gested that smaller population sizes of threatened species were variation in free-ranging populations of the Takahē (Porphyrio largely responsible for this relationship and that bird species at risk hochstetteri), an endangered flightless New Zealand rail (Grueber were relatively depauperate in terms of neutral genetic diversity. and Jamieson ), and in White Storks (Ciconia ciconia) in Sweden Ultimately, results of conservation genetic efforts for popu- (Olsson ). lations are used in defining units for conservation. These discus- Population connectivity and metapopulations.—A metapo- sions are often confusing because there are legal designations of pulation is a group of spatially segregated, but demographically populations under the ESA (i.e., DPSs; USFWS and National Ma- interacting (“connected”), populations. It is a useful concept for rine Fisheries Service ) and there are overlapping terms used understanding avian population structure and dynamics, even in the conservation literature to describe conservation units (e.g., in migratory species in which populations are not spatially dis- Ryder , Moritz ). Molecular markers can greatly aid both crete throughout the annual cycle (Esler ). However, not efforts, but distinctions between the two aspects of describing all fragmented populations behave as metapopulations; thus, populations of concern must be understood. Often broken down genetic data can be used to infer a population’s spatial organi- into ESUs and management units (MUs), there are many ways to zation (e.g., patchy populations, metapopulations, or isolated describe conservation units, but none of these have a legal basis populations; Mayer et al. ). Estimating metapopulation for protection (Fraser and Bernatchez ). Conversely, DPSs connectivity or sex-biased dispersal patterns (recently reviewed carry legal protection for the areas and species identified. The US- for all taxa by Broquet and Petit ) is an important aspect of FWS has come to depend more and more on molecular evidence conservation genetics because it helps identify factors contrib- for ESA–DPS decisions as the costs of generating the data decline uting to the decline of effective population size (i.e., species sta- and the need for better quantification of population boundaries tus). In the past, avian dispersal has been measured indirectly, increases (Fallon , Kelly ). via analysis of band returns (Crochet ), or via use of mito- Small populations: Pedigree analyses.—Pedigree analyses, chondrial DNA or limited numbers of microsatellite markers. which combine direct observations, molecular markers, and Thus, the chance of finding markers that track specific popula- pedigree models, have been underutilized in avian-conservation tions or individuals within them was considered quite slim, even efforts for wild and captive populations (Haig and Ballou , if there was some degree of population differentiation. However, Kruuk and Hill , Pemberton ). The paucity of microsat- fast-throughput sequencing changes this paradigm and opens ellites identified in bird studies (Primmer et al. ) prior to de- a new chapter in our ability to track birds at multiple temporal velopment of fast-throughput sequencing rendered this approach and spatial scales. limiting for avian applications because there was not enough sta- Regardless of the marker, many bird species, particu- tistical power to differentiate among individuals, particularly larly migratory species, exhibit low levels of population genetic closely related individuals. However, high-throughput sequencing structure because their ability to fly makes them good dispers- technology now provides access to far more microsatellite mark- ers (Crochet ). Thus, although habitat fragmentation has ers and single-nucleotide polymorphisms (SNPs) for these impor- been a major focus in conservation biology, it has had little de- tant analyses (inset ; Anderson and Garza , Backström et tectable effect on genetic structure in most recent avian studies al. , Hauser et al. ). Field observations and sampling of (e.g., Brown et al. , Funk et al. b, Barnett et al. , many full families can also add confidence to molecular pedigree Draheim et al. ). Barnett et al. () interpreted a lack of assessments; however, caution is warranted if the mating system genetic structure among habitat fragments as evidence for ongo- is not well understood (Charmantier and Réale , Wang and ing gene flow. However, potential “time lags” between the onset Santure ). of habitat fragmentation and their ramifications for population Despite these cautions, molecular pedigree assessments have connectivity were not considered. Care is required when evaluat- yielded important information about reductions in effective popu- ing evidence for ongoing connectivity of populations, especially lation size in wild animals (Slate , Sillanpää ). Townsend if the populations in question are not at migration–drift equi- () found disease-mediated inbreeding depression in a wild librium (Crochet ). Segelbacher et al. () addressed this population of cooperative American Crows (Corvus brachy- problem by sampling populations with different levels of spatial rynchus), and Ortego et al. () identified the importance of un- discontinuity (i.e., continuous range, metapopulations, isolated derstanding individual genetic diversity as it is related to clutch populations) and temporal isolation (recent vs. long isolated) to size and egg volume in small populations. Inbreeding avoidance determine how much genetic differentiation had accumulated. or lack thereof has also been investigated in a number of stud- By contrast, nonmigratory bird species may exhibit high levels of ies (e.g., Keller and Waller , Hansson et al. , Grant and differentiation and thus be more amenable to “traditional” stud- Grant , Keller et al. , Jamieson et al. , Szulkin et al. ies of population structure. For instance, Galbusera et al. () , Bush et al. ). successfully used assignment tests with microsatellite loci to In principle, once molecular markers identify genetic relat- identify individuals descended from migrants in recently isolated edness among pedigree founders and confirm parentage, pedi- populations of Taita Thrushes Turdus( helleri) and showed signif- gree models use the subsequent pedigree to evaluate the current icant genetic differentiation between the only three remaining status of a population, investigate strategies for reintroduction or subpopulations. APRIL 2011 — SPECIAL REVIEWS IN ORNITHOLOGY — 213
Recent reviews (Bossart and Prowell , Lowe and Allen- Several recent connectivity studies have gone beyond infer- dorf ) caution against making inferences about demographic ences based solely on genetic structure. Broquet et al. () pro- connectivity solely from genetic data and recommend using te- posed a model to estimate direct migration rates by comparing lemetry or mark–recapture data to validate such conclusions. genotypes of a population before and after dispersal. This model For instance, Fedy et al. () employed genetic and telemetry did not require migration–drift or Hardy-Weinberg equilib- methods to study connectivity among populations of White- rium and was robust even when few microsatellite markers were tailed Ptarmigan (Lagopus leucura) and found that although ge- available. However, it has not yet been applied to avian taxa and netic data suggested moderate gene flow between sites, telemetry performs best when a high proportion of individuals from each data did not capture the movement of any individuals between population are sampled. Peery et al. () used parentage as- populations. Mayer et al. () used banding surveys in con- signments and demographic simulations to evaluate the role of junction with nine microsatellite loci to quantify connectivity immigration in sustaining a threatened population of Marbled and identify which spatial model (patchy populations, metapop- Murrelets (Brachyramphus marmoratus). Microsatellite geno- ulation, isolated populations) best explained movement patterns types were used to estimate the number of parent–offspring pairs of Reed Buntings (Emberiza schoeniclus). Rollins et al. () within the population compared to numbers expected under dif- used microsatellite loci to study invasive European Starlings ferent models of immigration (i.e., a closed population versus a (Sturnus vulgaris) in Australia and were able to verify the source sink population). A related study compared historical and current population of new invasions, validate the existence of a sex-bi- genetic structure in those populations and found that migrants ased dispersal system, and confirm that gene flow between sub- were significantly less likely than resident birds to be involved in populations would make complete eradication of a population parent–offspring pairs and, thus, unlikely to rescue the declining difficult, necessitating continual management. Similarly, Barri- populations (Peery et al. ). By focusing on individuals rather entos et al. () used molecular markers to track movements than population genetic structure and not assuming equilibrium, of Trumpeter Finches (Bucanetes githagineus) throughout the such methods promise new insights into contemporary levels of annual cycle and across populations to document new popula- connectivity (Palsbøll et al. ). tion formation. They determined that movements of individuals Genetic data can be used to infer whether the current spa- toward sites outside their current range during the nonbreed- tial organization of populations reflects historical population ing season are likely to precede the establishment of new breed- structure or results from anthropogenic habitat fragmentation ing sites at the periphery of the distribution range. Conversely, (inset ; Segelbacher et al. , Miller and Haig ). More- Funk et al. (b) measured adequate gene flow among Great over, if we can measure the effect of historical habitat connec- Basin and Pacific Coast Snowy Plovers (Charadrius alexandri- tivity or fragmentation on gene flow, we will be better equipped nus), but banding information suggested quite minimal move- to make predictions regarding the effect of future climatic or ment between these inland and coastal areas. As a result, a DPS habitat conditions on gene flow and population viability (Hoe- was defined under the ESA on the basis of demographic isolation lzel ). rather than genetics. By linking demographic data with genetic data, cryptic pop- Dispersal abilities are particularly high among migratory ulation processes may emerge that are not evident when looking birds, in which long-distance movements, high dispersal rates, at these factors in isolation (Peery et al. ). Genetic identi- and high rates of gene flow can minimize genetic differentiation fication of a new and distinct population of the secretive Black of populations (Grinnell , Wetmore , Böhning-Gaese Rail (Laterallus jamaicensis) in the Sierra Nevada of northern et al. , Belliure et al. in Winker b). This is particu- California resulted in reconsideration of conservation priorities larly true in North America because repeated population isolation for the species (Girard et al. ). Incorporating genetics into and expansion associated with Pleistocene climatic fluctuations metapopulation viability analyses may also allow one to assess has played an important role in structuring intraspecific genetic the extent to which facilitating gene flow may slow the loss of variation in northern temperate birds (Avise and Walker , heterozygosity and alleviate the projected effects of inbreeding Klicka and Zink , Milá et al. , Klicka et al. ). This depression (Pienkowski et al. , Segelbacher and Storch , has resulted in low resolution when using standard approaches for Schiegg et al. ). measuring connectivity, such as estimating gene flow among pop- Metapopulation management: Translocations and reintroduc- ulations or identifying individuals dispersed from other popula- tions.—Translocations and reintroductions can be used to () tions (called “migrants” in the population genetics literature) via supplement small or declining populations; () re-establish popu- population assignment tests. lations within their historical range; or () establish populations In one of the first studies of avian population structure to in novel areas (i.e., assisted migration and colonization) because use high-throughput sequencing, Li and Merilä () identified their historical range is, or is likely to become, uninhabitable as a microsatellite markers across the Siberian Jay (Perisoreus in- result of climate change, invasive species, habitat destruction, or a faustus) genome and used them to examine sex-biased disper- nexus of other threats. From a conservation genetics perspective, it sal. They estimated the scale at which linkage disequilibrium is best to augment or re-establish metapopulations with individu- among markers decayed for each sex. Because () males had als from populations that were connected historically by gene flow lower heterozygosity and () linkage disequilibrium decayed to reduce the chances of outbreeding depression and to increase much faster for females, they concluded that dispersal is female the chances of retaining genomic components that reflect local biased (but did not estimate the geographic distances over which adaptation (Storfer ; but see Jacobsen et al. ). Currently, this occurred). evidence of avian outbreeding depression is scarce (Frankham et al. 214 — SPECIAL REVIEWS IN ORNITHOLOGY — AUK,VOL. 128
; but see Marr et al. ) and predicting the risk of its occur- life cycle or throughout an animal’s life cycle (Webster et al. , rence is one of the most important unmet scientific challenges in Marra et al. ; see www.migratoryconnectivityproject.org). the field of conservation genetics (Frankham ). In small popula- Long seasonal migrations of many temperate bird species con- tions, reducing the risk of outbreeding depression must be balanced found some of the traditional interpretations of connectivity ap- against the need to minimize inbreeding (Keller and Waller ) plied to other taxa, in which it is primarily defined as movements and manage genetic variation to facilitate long-term persistence of between “suitable patches” that serve as year-round or breeding the source and target populations (Haig et al. ). In extreme cir- habitat (Hilty et al. ). By contrast, migratory birds may ag- cumstances (e.g., when a species would otherwise go extinct), in- gregate differently in winter and breeding habitats, with poten- tercrossing different but closely related taxa or ESUs (i.e., genetic tial for genetic structure depending on whether pairing occurs rescue; Tallmon et al. ) may be the only method for preserving during migration or on the breeding grounds (Flint et al. , portions of an imperiled species’ genome (Tarr and Fleischer , Winker b). Genetic approaches to investigating migratory Tallmon et al. , Hedrick and Fredrickson ). In translocat- connectivity have been most effective when integrated with band- ing individuals into small populations, one must always consider ing surveys, satellite telemetry, and isotope analysis (e.g., Clegg the potential for complete replacement of small gene pools by ge- et al. , Hobson , Kelly et al. , Hellgren et al. ), netically more diverse individuals that may be more fit (i.e., genetic although stock identification (matching individuals to breed- swamping; Bouzat et al. ). Thus, demographic challenges need ing populations based on genetic assignment) at overwintering to be addressed prior to genetic considerations (Frankham et al. grounds has succeeded in some cases (Haig et al. ). For exam- ), and risk analysis of options is usually advisable. ple, Sonsthagen et al. () identified hierarchical spatial genetic Where there is significant uncertainty in the genetic makeup structure in Common Eiders (Somateria mollissima) breeding of source or donor populations for translocations, and where the along a migratory corridor. Likewise, Wenink et al. () used effects may be irreversible, moving individuals can be tantamount mitochondrial DNA lineages of Dunlin (Calidris alpina) at winter to ecological gambling and counter to the precautionary princi- sites to assign individuals to their population of origin. Pearce ple in conservation biology (sensu Ricciardi and Simberloff ). et al. () used microsatellite genotypes and mitochondrial Yet, in the crisis discipline of conservation biology, risk manage- DNA from Canada Geese (Branta canadensis) collected at hunter ment requires that one weigh the risk of inaction against the risk check stations to determine how harvest was affecting similar- of action. A genetic assessment of intra- and interpopulation dif- appearing subspecies or populations with different conservation ferentiation prior to translocations can help quantify uncertainty status (i.e., declining or stable). Cadiou et al. () attempted to and risk associated with artificially creating gene flow, evaluate assign breeding origin to Common Guillemots (Uria aalge) that the appropriateness of alternative population sources or targets died in a massive oil spill at their wintering grounds using micro- (e.g., Haig et al. ; Tarr and Fleischer , ), and set pri- satellite data. The characteristic limitation imposed by weak genetic orities for conservation of genetic diversity (Haig et al. , Boes- structure prevented accurate genetic assignment, but Cadiou et senkool et al. ). al. () concluded that the die-off was unlikely to cause loss of Following implementation of translocations, genetic assess- much genetic diversity, given that genetic structure was so weak. ments can measure whether the movement of animals met ge- Flint et al. () used the lack of genetic structure, in combination netic or demographic management goals. For example, Bouzat with banding returns, to determine that populations of Pintails et al. () found that translocations of Greater Prairie Chick- (Anas acuta) in North America and Asia routinely exchange mi- ens (Tympanuchus cupido pinnatus) were an effective tool in de- grants in numbers irrelevant to demography but sufficient to allow creasing inbreeding coefficients and increasing genetic diversity gene flow and, perhaps, transmission of parasites. while not swamping the genetic makeup of the target population. On the other hand, Hall et al. (), in an extension of the Conversely, translocations of New Zealand’s South Island Rob- novel approach employed by Peery et al. (), estimated the pro- ins (Petroica australis australis) to island refugia resulted in high portion of migrants at different seasons in a peripheral population levels of inbreeding, low levels of genetic diversity, and higher of Marbled Murrelets using assignment tests from microsatel- hatching failure rates, which suggests that future translocation lite markers. They used simulations to determine threshold levels efforts warranted more careful consideration of founder compo- of significance for identifying migrants that balanced Type I and sition and numbers (Boessenkool et al. ). Talbot et al. () Type II error and estimated the reproductive contribution of those discovered that translocation of Dusky Canada Geese (Branta migrants by identifying possible parent–offspring pairs involving canadensis occidentalis) to augment a population on Middleton migrants and comparing those with expectations generated from Island in the Gulf of Alaska was not effective because subsequent demographic models. Despite low genetic structure between pe- population increases were determined to be the result of immi- ripheral (central California) and source (Alaska) populations, which gration from other islands rather than translocated geese. This could have precluded direct estimation of migration rates from as- finding would have gone undetected without an understanding signment tests, they concluded that most migrants were females of population structure from genetic markers. Finally, a severe and the population was composed of a high number of migrants in population bottleneck suffered by captive White-headed Ducks the winter, but few migrants were present during breeding seasons (Oxyura leucocephala) led Muñoz-Fuentes et al. () to recom- and there were few individuals of mixed ancestry. This approach re- mend that more genetically diverse populations be established in quired assumptions about the demographic history of the popula- captivity and the wild. tion but demonstrated a potential solution to the typical problem Migratory connectivity.—Migratory connectivity is the geo- that assignment tests are most reliable for detecting migrants only graphic linking of individuals or populations between stages of a when there is strong genetic structure (i.e., very low migration). APRIL 2011 — SPECIAL REVIEWS IN ORNITHOLOGY — 215
Because avian migrations have important implications for in high-latitude geographic regions and those that inhabit more the transmission of disease, recent studies have also used genetic equatorial or tropical locales. information from parasites to illuminate interactions among host High-latitude locales.—Most avian species that use high- populations. Waldenström et al. () sequenced mitochondrial latitude breeding areas migrate to lower latitudes during winter. DNA of hemosporidian parasites harbored by migratory songbirds The mobility of such taxa suggests that prospects for detecting and determined that some parasites were more likely acquired interesting patterns of genetic structure across landscapes should on African overwintering grounds than on European breeding be low. In these cases, if genetic investigations are performed, one grounds. Koehler et al. () conducted phylogenetic analyses of three possible outcomes may be observed: () complete pan- of avian influenza strains isolated from migratory Northern Pin- mixia (no genetic structure; e.g., Veit et al. ); () isolation-by- tails and concluded that transcontinental migration facilitated distance (i.e., significant correlations between geographic distance coinfection by, and reassortment of, multiple strains of influenza. and genetic distances of breeding populations; e.g., Draheim et al. Although those studies were more focused on determining the ); or () subspecies-level differences among groups of breed- source of particular infections, other studies have attempted to ing populations, coupled with the potential for either panmixia or identify breeding grounds on the basis of hemosporidian parasite isolation-by-distance within each subspecies group (e.g., Miller et assemblages in migratory birds (e.g., Fallon et al. , Pagenkopp al. ). In the latter case, genetic structure across space may be et al. ). However, these studies require highly differentiated, more likely to result from geographic separation of populations geographically distinct parasite lineages and have had limited suc- rather than particular aspects of landscapes per se. Inevitably, the cess to date. likelihood of each outcome depends on the degree of natal- and Finally, high-throughput sequencing and other high-resolu- breeding-site fidelity demonstrated by the species under investi- tion methods (e.g., microarrays) will increase our ability to find gation. Furthermore, these patterns may be apparent only when population-specific markers to track bird populations (inset ). breeding population samples encompass extremely large (e.g., Even so, analyses will be more successful if only markers that dif- continent-wide) spatial extents. Thus, landscape-level features will ferentiate or suggest population differentiation are used to search probably not have a tremendous influence on species that inhabit for migratory patterns. Often, all markers are used in assignment high latitudes. tests, which results in less than definitive patterns, although all Despite this assertion, several studies have successfully im- variable markers will be informative if dispersal measures that plemented landscape genetic concepts and approaches, indicat- rely on estimating kinship are employed. ing that exceptions to the three scenarios stated above can occur. For example, analyses of the Golden-cheeked Warbler (Dend- LANDSCAPE GENETICS roica chrysoparia) by Lindsay et al. () identified significant associations between genetic structure patterns and variables Landscape genetics is a relatively new discipline that has gained that encompassed population connectivity, forest fragmenta- tremendous popularity in recent years (Manel et al. , Storfer tion, and the percentage of agricultural land between breeding et al. ). Landscape genetic approaches extend numerous con- populations in Texas. Although the Golden-cheeked Warbler is ventional population genetic analyses in a manner that provides a migratory species, the patterns observed in that study may be identification of the effects of landscape features and landscape attributable to highly specific breeding-habitat requirements, a heterogeneity on genetic diversity and structure patterns within low overall number of breeding adults, and short dispersal dis- or across species (Miller et al. , Safner et al. ). In addi- tances between natal sites or the previous year’s breeding sites. tion to having conservation implications and improving our un- Furthermore, patterns from D. chrysoparia contrast starkly with derstanding of evolutionary ecology, landscape genetic analyses the absence of genetic structure in the Cerulean Warbler (D. ce- can further be used to examine topics such as disease transmis- rulea; Veit et al. ), a congener that migrates over longer dis- sion across a landscape (Ekblom et al. ) and climate change tances to breed throughout the more heavily forested regions of (see below). A November search of the term “landscape ge- central and northeastern North America. Genetic structure in netics” using ISI’s Web of Science revealed more than papers Wrentits (Chamaea fasciata) across habitat fragments isolated by since that claimed to deal with this topic (as either self- urbanization in southern California was surprisingly strong and reported by authors’ key words or as annotated by ISI’s “keywords concordant with levels of structure found in other, less mobile, plus” feature). Storfer et al. () identified published studies vertebrates (Delaney et al. ). that included at least one landscape-level variable when interpret- Among avian taxa that inhabit higher latitudes, galliforms ing genetic structure patterns. Interestingly, fewer than of these may be the best candidates for landscape genetic investigations, studies involved birds (A. Storfer pers. comm.). because of their low dispersal compared with other avian taxa Prospects for landscape genetic investigations in avian taxa.— (Barrowclough et al. ; Oyler-McCance et al. a, b; Spauld- Many, if not most, avian taxa have the ability to circumvent or ing et al. ; Fedy et al. ) and strong associations with spe- rapidly traverse landscape features that may disrupt or influ- cific habitat types in some species of grouse (Braun et al. , ence genetic structure patterns in less vagile organisms. Superfi- ; Zwickel and Bendell ; Hoffman ). For example, cially, this attribute suggests that birds are not necessarily useful landscape genetic analyses applied to Capercaillies (Tetrao urogal- model species for landscape genetic investigations. Despite this lus; Braunisch et al. ) in the Black Forest of Germany revealed assertion, we suggest that prospects exist to perform meaningful numerous loose correlations between genetic structure and land- landscape genetic analyses for many avian taxa. As a conceptual cover variables, including forest habitat quantity, forest edges, ag- framework, we consider two geographic extremes: taxa that breed ricultural lands, and roads. 216 — SPECIAL REVIEWS IN ORNITHOLOGY — AUK,VOL. 128
Equatorial and tropical locales.—At lower latitudes, most Outcomes from landscape genetic investigations may ad- bird species are nonmigratory and demonstrate low dispersal ten- vance evolutionary ecology theory and promote development of dencies and, sometimes, reduced flight capabilities (Wallace , new hypotheses. For example, identification of associations be- Janzen , Moore et al. , Kerr et al. , Ibarra-Macias tween landscape characteristics and patterns of genetic structure et al. ). Many of these species also demonstrate higher levels should generate hypotheses to explain the occurrence of such as- of genetic differentiation across geographic space than taxa from sociations. We know, for example, that limited dispersal across more temperate climates, despite often inhabiting smaller geo- tropical mountains or large rivers can create substantial spatial ge- graphic ranges (Brown et al. and references therein, Fran- netic structure (Capparella , Brumfield and Capparella ) cisco et al. , Burney and Brumfield ). These patterns and that different species have varying abilities to move across reflect the generalized “latitudinal biodiversity gradient,” which some habitats (Moore et al. , Ibarra-Macias et al. ). Those occurs at the interspecific level (Stevens ), among subspecies patterns lead to questions about what inhibits movements of some (Martin and Tewksbury ), and even within individual popu- taxa across geographic space (i.e., neophobia) while not limiting lations (Wikelski et al. ). Latitudinal diversity gradients are movement of other taxa (Stratford and Robinson , Burney increasingly being addressed with the use of molecular markers and Brumfield ). Identification of ecological characteristics (e.g., Martin and McKay ), and the results suggest that mo- associated with limited movement can predict levels of genetic lecular diversity may parallel taxonomic and phenotypic diver- structure, even without extensive genetic data, and can help iden- sity. Explanations for latitudinal diversity gradients encompass tify taxa that are likely to be sensitive to the effects of isolation, for a variety of factors, including () historical climatic oscillation example that resulting from forest fragmentation (Stratford and (Dynesius and Jansson ), () temperature kinetics (Wikelski Robinson ). A wide variety of interesting behavioral or physi- et al. , Allen et al. ), and () the greater efficacy of riv- cal mechanisms could account for limited movements and may ers and mountains as barriers in the tropics than in temperate result from lower visual acuity of forest birds entering pasture or locales (Janzen , Brumfield and Capparella , Bates et al. grassland habitats, limited physiological capacity for sustained ). Of these factors, the last will most likely have the great- flight, behavioral aversion to open habitats because of perceived est effect within species. Consequently, in addition to potentially predation risk, or even limited plasticity of physiological capacity observing panmixia, isolation-by-distance patterns, and subspe- when moving through unusual habitats (Harris and Reed , cies-level differences at different spatial scales, we suggest that Stratford and Robinson ). analyses of tropical and equatorial avian taxa will harbor greater Finally, because landscape genetic studies provide insights prospects for identifying signatures of landscape attributes on ge- toward the degree of population connectivity and factors that netic structure patterns. promote it, results can help develop a better understanding of the Despite recent interest in landscape genetic approaches, rela- dynamics of disease vectors and the spread of human and avian tively few studies have applied these concepts and techniques to diseases (Archie et al. ). The classic example of this is the tropical and equatorial bird species. That said, molecular mark- spread and effect of malaria on the birds of Hawaii (e.g., Beadell ers have highlighted the effects of forest fragmentation in several et al. , Foster et al. , Eggert et al. , Jarvi et al. ). cases (Bates , ; Brown et al. ; Reding et al. ). The introduced Southern House Mosquito Culex( quinquefascia- The potential effect of deforestation in tropical systems is well es- tus) is the principal vector of avian malaria (Plasmodium relic- tablished. However, human-induced forest fragmentation will, tum; Fonseca et al. ). Endemic birds of Hawaii have variable in most cases, result in relatively new sets of landscape features. and relatively low resistance to this introduced malaria (van Riper Consequently, studies that include historical and current range , Atkinson and Samuel ), although for most non-native patterns in analyses (e.g., Pavlacky et al. , Reding et al. ) species it is relatively benign. Currently, this mosquito occurs at may not only shed light on the genetic consequences of fragmen- or below , m, and nearly all native Hawaiian bird species that tation itself, but also provide unique opportunities to discern the once occurred at or below this elevation no longer do. As the mos- time scales over which the effects of such perturbations become quito moves to higher elevations because of climate change, in- detectable within natural populations. trogression from more cold-tolerant mosquito species, or both Why perform landscape genetic investigations?—Given the (Fonseca et al. ), more species will likely become exposed to growing application of landscape genetic approaches, we antici- this disease (Atkinson and Samuel , State of the Birds ). pate that there likely will be an appreciable increase in the number Genetic sampling of mosquitoes across landscapes of varying el- of such studies performed on avian species in the near future. As evations could provide a key to the location and direction of ex- with all landscape genetic investigations, these efforts will provide pansion of infected mosquitoes (Fonseca et al. , Keyghobadi more detailed insights into the factors that influence genetic di- et al. ). versity and structure at different spatial scales. We suggest numer- ous additional benefits, including identification of cryptic species, EMERGING APPLICATIONS ESUs, subspecies, etc., that help prioritize important habitat for conservation. Of particular importance will be the identification Climate change.—Measuring, predicting, and planning to miti- of habitat types that can help promote connectivity and minimize gate the effects of climate change on wildlife species is of para- population fragmentation (Braunisch et al. ). These insights mount importance (Intergovernmental Panel on Climate Change may be enhanced if composite patterns from multiple species are ). Fortunately, there are a number of genetic approaches that considered simultaneously, because such efforts may help priori- can offer direct and indirect contributions to this aspect of avian tize habitat requirements for entire suites of taxa within a geo- conservation. A directionally changing environment capable of graphic region (Vandergast et al. , Miller and Haig ). producing massive demographic shifts is also capable of producing APRIL 2011 — SPECIAL REVIEWS IN ORNITHOLOGY — 217
a massive selection event (Skelly et al. ). Although the rapid at greater risk or those that might be more likely to succeed using phenotypic and behavioral changes we are witnessing may be a approaches such as translocations or reintroductions. function, in many cases, of phenotypic plasticity rather than adap- Ecotoxicology.—Ecotoxicological research has linked a broad tive evolution (Gienapp et al. ), there are growing examples taxonomic spectrum of avian population declines with exposure of rapid adaptive evolution in response to climate change in birds to numerous classes of contaminants, including (but not limited (reviewed in Sheldon ). In a selection experiment with Black- to) DDT and other organochlorine compounds (Ratcliffe ), caps (Sylvia atricapilla), Pulido and Berthold () demonstrated mercury (Burgess and Meyer ), lead (Meretsky et al. ), that nonmigratory Blackcaps were found in a completely migra- selenium (Ohlendorf and Hothem ), agricultural pesticides tory population after only two generations of directional selection (Goldstein et al. , Mora ), and polycyclic aromatic hydro- for lower migratory activity. The strong evolutionary reduction in carbons (Iverson and Esler ). Although the mitigation of ex- migration distance found in that study is in line with the expected posure sources subsequently facilitated recoveries in some cases, adaptive changes in bird migration in response to environmen- the potential long-term effects on population structure, particu- tal alterations caused by climate change (Bradshaw and Holzapfel larly population bottlenecks, are unclear. Modern genetic tech- , ). niques (as described throughout this review) offer powerful tools Molecular markers that track genetic patterns across popula- to quantify a range of effects related to contaminant exposure tions or landscapes can help predict future rates of genetic changes and identify groups of birds that may face substantial risk of in modified landscapes. One might predict that species (lineages) deleterious effects. with higher genetic diversity would respond more rapidly to envi- Although originally focused on narrow, single-species stud- ronmental variations along “leading” edges of ranges as climate ies and overt symptoms of toxicity resulting from ecologically ir- changes. For example, climate predictions for the Pyrenees Moun- relevant exposures, the field of ecotoxicology has experienced a tains of Western Europe include further fragmentation of the “sky renaissance in developing a broader, more integrated understand- island” alpine habitat used by Rock Ptarmigan (Lagopus muta). Beck ing of the direct and indirect effects of contaminants on ecosys- et al. () discovered genetically isolated and depauperate popu- tem function that span molecular to ecosystem scales of biological lations that may need translocation if current habitat fragmenta- organization (Snape et al. , Newman and Clements ). tion continues. A multispecies study currently underway examines Yet despite these advantages, applications of genetic techniques the effects of climate change on wetlands and waterbirds in the to population- or landscape-scale ecotoxicological issues has Great Basin (S. M. Haig et al. unpubl. data). Genetic structur- lagged far behind other disciplines traditionally addressed in con- ing in highly vagile waterbird populations across this region is not servation genetics. Furthermore, avian taxa have been relatively strong enough to use molecular markers to monitor changes over neglected with respect to conservation genetic approaches to con- a short time frame, but examining how ecological shifts across the taminant effects in comparison with other taxonomic groups, landscape may affect the distribution, dispersal, and genetics of such as fish, amphibians, and invertebrates. The specific reasons their aquatic prey species can be informative. for these research patterns are unclear but are likely attribut- Despite advances in many areas of genetics, the potential for able in part to the reductionist history of ecotoxicology (focus on evolutionary responses is rarely considered in bioclimatic mod- mechanisms of damage as opposed to emergent effects of expo- els of species’ range shifts (Pearson and Dawson , Skelly et sure) as well as the seeming intractability of linking contaminant al. ), even though such models are among the primary tools exposure with latent responses in avian population genetic struc- being used to assess potential effects of climate change on spe- ture, particularly in the face of numerous other influencing fac- cies distributions (e.g., Stralberg et al. ). Assuming that there tors related to avian vagility. However, substantial progress could will be no evolutionary response to climate change may result in be made in our understanding of how long-term contaminant ex- overly pessimistic predictions, especially for species that disperse posure may influence population-level processes in wild birds by long distances, are under selection at range margins, or have short merging many of the conservation genetic approaches described generation times that facilitate more rapid intergenerational se- throughout this review with a robust assessment of contaminant lection. Therefore, the most appropriate application of predictive exposure at various life stages within an evolutionary toxicology bioclimatic envelope models may be for long-lived species that are framework (Staton et al. ). poor dispersers (Pearson and Dawson ), although Tingley et Contaminants can influence individual and population genetic al. () found that % of bird distributions resurveyed after structure by directly damaging genetic material (Skarphedinsdottir years in the Sierra Nevada of California indicated changes in their et al. ) or through selective effects of chemicals on gene fre- climatic niches. Development of more mechanistic models that quencies within exposed populations (Theodorakis et al. ). incorporate the potential for an evolutionary response and predict It is the latter effect to which conservation genetic approaches are evolutionary responses in tandem with ecological responses may most aptly applied. Because individuals often vary in their sen- provide additional realism and improve predictive strength (Skelly sitivity to various contaminants, chronic exposure may result in et al. , La Sorte and Jetz ); however, doing so will require fitness costs (e.g., reduced survival, impaired reproduction, or that we develop better molecular tools for measuring a species’ compromised immune response; Belfiore and Anderson ) in potential for adaptive variation in novel environments (Scoble and sensitive individuals. Thus, one would expect to see directional Lowe ). Recent technological advances in genomics allow for selection for tolerant genotypes if such susceptibility had a ge- not only the expansion of the amount of the genome examined netic basis. Unfortunately, attributing these types of responses but also the detection and characterization of functional genes to contaminant exposure among avian populations is exceed- that are responsible for survival and adaptation in such cases. This ingly difficult because of their relatively long life spans and high knowledge could help managers determine which species could be dispersal abilities. 218 — SPECIAL REVIEWS IN ORNITHOLOGY — AUK,VOL. 128
Contaminant exposure may reduce overall genetic diver- loci. Furthermore, over the past two decades, developments in ex- sity within populations by reducing the effective population size, amining ancient DNA have opened a completely new window into especially if barriers to gene flow exist (Evenden and Depledge examining avian evolutionary and demographic history. The near ). Possible approaches for evaluating these potential effects future promises that an understanding of the complete genome require a general understanding of background population ge- of an individual or individuals across space and time will provide netic structure and comparisons of genetic diversity between nu- a deeper understanding of issues related to the effects of disease, merous exposed and unexposed populations or along gradients toxins, population bottlenecks, and other processes on species, of exposure. Whitehead et al. () employed this approach us- populations, and landscapes. The challenge for avian conserva- ing AFLP and microsatellite markers in native fish species to test tion geneticists is to understand how this new technology can be whether patterns of genetic variation were consistent with long- applied to answering critical questions related to avian conserva- term pesticide exposure or with expectations based on biogeog- tion. We offer the following insights and perspectives for moving raphy. Agricultural systems are particularly promising areas in forward. which to apply these approaches because they support a broad () Taxonomy is critical to conservation because it defines el- range of avian taxa, regularly receive generous doses of various ements of biodiversity. Since its inception as a field of study, ge- herbicides and insecticides, and can often be studied with suit- netics has played a critical role in identifying and grouping taxa, able replication. However, assessing population-level risk from and we expect that this role will continue to expand with advances exposures on the basis of genetic diversity may be the most prom- in genomics. However, philosophical differences regarding how to ising application of conservation genetic tools to contaminant re- recognize and define species, subspecies, and appropriate popula- search. Small, isolated populations that already have low genetic tion units for conservation need to be resolved. variability are likely to be more vulnerable to external stressors () Traditional genetic tools have been, and continue to be, such as toxic compounds, particularly if coupled with other bar- successfully applied to a host of avian conservation issues, includ- riers to gene flow. Integrating contaminant exposure research ing improved assessment of population structure, gene flow, and with assessments of genetic structure can help prioritize man- pedigrees. Genomic approaches like the use of SNPs are likely agement efforts to preferentially reduce exposure in those popu- to increase the discriminative power of these analyses by or- lations that are least likely to have the genetic capacity to deal ders of magnitude, but a new wave of bioinformatic approaches with chemical stressors. will likely be necessary to handle the coming deluge of genetic Application of other emerging genetic tools, such as microar- information. rays (Lettieri ), will help further our understanding of the () Multiple data sets should be used to define taxa and mechanisms of contaminant effects. A deeper insight into how population structure. These temporal and scalar comparisons various classes of contaminants induce or alter gene expression can be key to understanding what type of conservation action is and the associated phenotypic responses will provide better un- warranted. derstanding of individual-level effects, identify species-specific () Incorporation of historical specimens (e.g., museum skins sensitivity profiles, and help develop effective biomarkers of both and subfossils) into genetic studies has revolutionized all major exposure and effects. These approaches are now relatively com- subdisciplines of taxonomy and population genetics that benefit mon among fish, amphibian, and invertebrate taxa and merely from a direct historical perspective. await application to avian species. () Molecular markers can identify cryptic species and The abundance of published avian conservation genetic and population processes that cannot be observed in any other avian ecotoxicology studies highlights the importance of these way. Thus, they warrant consideration in most conservation two disciplines. Yet the dearth of current research linking them investigations. suggests the existence of a critical information gap and a clear area () The emerging field of landscape genetics can play a critical for research merging these issues. A logical starting point is to pair role in determining the effects of past, present, and future climatic comparisons of genetic diversity among populations with a range and land-use changes on species and their populations. of tissue contaminants in order to build data sets that can be used () Ecotoxicological and genetic approaches to studying con- to test some of these hypotheses. Species with broad monitoring taminant issues have yet to be widely integrated into avian studies networks to build upon (e.g., Tree Swallows [Tachycineta bicolor], but could prove insightful. Wood Ducks [Aix sponsa], and Purple Martins [Progne subis]) Ultimately, biodiversity conservation requires preservation may be particularly useful for these initial efforts. However, care- of as much variation as possible at all taxonomic levels. To real- ful study design is imperative to sufficiently address other drivers ize that goal, conservationists and geneticists need to maintain of fitness or genetic diversity and minimize the potential for spu- open lines of communication to design and implement strategies rious results. to help the world’s marvelously rich assemblage of birds endure the current and future state of biodiversity triage. PERSPECTIVE ACKNOWLEDGMENTS Molecular technology continues to evolve at an ever increasing pace. Recent development of high-throughput DNA sequencing We are grateful to R. Fleischer and several anonymous review- has revolutionized our ability to examine hundreds of thousands ers for comments on the manuscript. We further thank the U.S. of variable markers, whereas less than years ago, avian geneti- Geological Survey (USGS) Forest and Rangeland Ecosystem Sci- cists were content with analyzing to variable microsatellite ence Center, Oregon State University, USGS Fort Collins Science APRIL 2011 — SPECIAL REVIEWS IN ORNITHOLOGY — 219
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