The Auk 109(4):828-846, 1992
PHYLOGENETIC
ANALYSIS
MARY
OF AVIAN
PARENTAL
CARE
C. MCKITRICK
Museumof ZoologyandDepartmentof Biology,Universityof Michigan,
Ann Arbor,Michigan48109, USA
ABsTRACT.--Phylogenetic
patternscan be usedto generatedetailedhistoricalhypotheses
about the evolution of charactersystems,including parental-carebehavior. Phylogenetic
analysisof 60 taxausingparental-caredata(15 characters)
in combinationwith anatomical
data (69 characters)showsthat biparental care is primitive for birds, and that biparental
incubationarosefrom an ancestralconditionin which neither parent incubated.Components
of parentalcaremaybe decoupled,suchthat incubationand feedingof nestlingsisbiparental,
but postfledgingcareis uniparental;the patternof decouplingvariesacrosstaxa.Behavioral
plasticity,environmentallyinducedvariation,and quantitativevariationin characters
that
arecodedqualitativelyaresomeof the problemsinherentin suchan analysis.Nevertheless,
historicalanalysisoffersa goodvehiclefor obtainingrigoroushypotheses
aboutthe coevolution of avian charactersystems.Received
5 July1991,accepted
29 October1991.
THEUSEof phylogeneticpattern to elucidate
questionsaboutother evolutionaryand ecological patternsor processeshas becomeincreasingly commonin the last 15 years.Severalrigorousattemptsto incorporatebehavioral data
into phylogeneticanalysesor to comparesuch
datawith existingphylogenieshavebeenmade
in the lastfive years.Clutton-Brockand Harvey
(1977) recognized the pitfalls of comparing
closelyrelated speciesto study the origin of
ecologicalphenomena,and this has been further emphasizedby Clutton-Brockand Harvey
(1979), Ridley (1978, 1983), Harvey and Mace
(1982),Felsenstein(1985),Dobson(1985), Pagel
and Harvey (1988),H/Sglund(1989),and Bj/Srklund (1990). Coddington (1988) outlined a
method for using cladistichypothesesof relationship to test hypothesesof adaptation,and
this kind of approachhas been fruitfully applied in a numberof recentstudies(Prum 1990,
B.N. Danforthunpubl. data,R. J.Smith unpubl.
phylogeny(oneof the "topthreeheinous'crimes
againstphylogenetics'"; Brooksand McLennan
1991). Looking at numerousspeciesfrom the
same taxonomic family actually may be quite
valid, dependingon phylogeneticrelationships
amongthosespecies.What mattersaboveall is
the number of times the trait in questionarose,
rather than how many genera or families show
the trait; this can only be determined by a detailed phylogeny of the organismsand traits.
data).
A historicalapproachis a profitable one, as
it attemptsto find the correcthierarchicallevel
at which hypothesesof adaptationare meaningful. It is not enough simply to dismiss"adaptations"as artifactsof phylogeneticpropinquity;rather, one mustdissectout the effectsof
phylogeny so that adaptive explanationsmay
be viewed in the appropriatecontext.CluttonBrockand Harvey's (1979) concernaboutbiasing investigationsof ecologicalphenomenaby
examining closely related specieswas appropriate. However, they may have been somewhat tyrannizedby taxonomyin their view of
the problem--that is, equatingtaxonomywith
828
The trait could well have arisen numerous
times
within the family, in which caseit is not only
meaningfulbut necessaryto include members
of the samefamily in the study. With such information, one can ask appropriate questions
aboutthe adaptivesignificanceof that trait. It
is not profitable to begin the investigationby
determiningwhether one shouldcountgenera,
families
or orders
in which
the trait
occurs.
Rather, one should begin with a detailed phylogeny and determine whether the trait arose
onceor many times, and the pattern of origin
and loss. Adaptive explanationscan only be
testedwith convergentcases,not with homol-
ogousones.In other words,two speciesshowing the trait can only serveas two data points
in supportof an adaptiveexplanationof origin
if they did not inherit the trait from a common
ancestor.
McLennan et al. (1988) lamented what they
perceivedasa declinein the useof behavioral
data to constructphylogenetic hypothesesin
the last three decades,citing work by Lorenz
(1941) in which this was done successfullyfor
ducks(Anatidae)and work by later authorsin
which phylogeny was ignored. A noncladistic
October
1992]
Phylogeny
ofAvian
Parental
Care
829
attempt to extend Lorenz's work was made by
Johnsgard(1961),for example.McLennan et al.
(1988) were remarkablysuccessfulin generating phylogenies for gasterosteidfishes using
data on reproductivebehavior,and argued that
behavioral data are extremely useful for constructing phylogenies.
The evolution of parental care was an early
focus of the phylogenetic approach. Ridley
(1978) reviewed the circumstancesof paternal
care in a broad array of taxa to consider the
effectsof fertilization mode, territoriality, fe-
Cracraft's (1981) classification, which lacks
dition in birds. His hypothesisis basedupon
These terms are relative, and the hierarchical
characterdata and explicit hypothesesof phy-
logeneticrelationships,is of limited utility for
the purposeof understandingthe evolutionof
charactersystems(e.g. behavior). Without a
phylogeny,van Rhijn was limited to making
hypothesesbased on statisticalprobabilities
rather than historical
evidence.
In this study, I use characterdata from the
hindlimb musculature (from McKitrick 1991) in
combinationwith publishedbehavioraldata to
test van Rhijn's hypothesisthat male-only pamale choice and other factors on the evolution
rental careis primitive in birds,and to generate,
of paternal care.He recognizedthe possibility in effect,phylogeniesof avian parental-carebeof phylogeneticbiasin formulatinghypotheses havior. In doing so,I alsowas able to test some
about the evolution of the phenomenon. Git- of the hypothesesof Silver et al. (1985) about
tleman (1981) used phylogeny to test predic- the causalnature of associationsamong certain
tions about probabilities of transition among aspectsof parental care. In considering the
typesof parentalcarein bony fishes(i.e. among question of what aspectsof parental care are
states of uniparental [male], uniparental [fe- primitive for birds,however,it shouldbe borne
male], biparental, and no parental care). He in mind that there is nothing magical about
foundthatthe mostcommonevolutionarytran- statementsregarding the primitive or derived
nature of these character states. A character state
sition was from no parental care to uniparental
care by males, but pointed out possiblestatis- that is derived for birdsis primitive within birds.
tical problems with the conclusion that this A statemaybe derivedfor birds,but showearly
transitions to a different state, such that the matransition had the highest likelihood.
Van Rhijn (1984, 1985, 1990) proposed that jority of birds show a different statefrom the
pure male parental care is the primitive con- one that aroseat the baseof the avian lineage.
the premise that "monogamouspaternal care
systemscan easily evolve towards all recent
mating systemsin birds" (van Rhijn 1984:103),
whereasbiparental caresystemscannot.This is
in contrastwith the suggestionby Emlen and
Oring (1977:220)that "complete male parental
care is most likely to develop in groupswith
... a phylogenetic history of shared incubation." If van Rhijn's hypothesisis correct,then
complete male care would probably have
evolved from a condition
where incubation
was
lacking,asin crocodilians
and possiblynonavian dinosaurs;van Rhijn, however, limited his
discussion
to birds.
level to which they refer shouldalwaysbe considered.
Phylogeniesare hypothesesabout character
evolution and, as such,they allow the refinement of ecologicalquestionssuchas,why does
speciesX exhibit biparentalcare?With a phylogeny,one can go beyondthe proximateanswer to this question,namely, "Becauseits ancestorsexhibited biparental care," and seek
ultimate answersby examiningthe ecological
parametersthat may have contributed to the
origin of biparentalcarein the variouslineages
in which it arose.My study is not an attempt
to poseand answer suchquestions,but rather
to begin to constructa historicalframework
within which suchquestionsmay be explored.
Van Rhijn (1990) attempted to support his
view primarily by using Cracraft's(1981) clasThe hindlimb musculature of birds has been
sificationof birdsand Strauch's(1978)phylogeny of the order Charadriiformes (shorebirds usedeffectivelyto generatecladistichypotheses
and allies). Testing van Rhijn's intriguing hy- for restrictedlineages(e.g. Old World subospothesis was somewhat hampered at the time cines;Raikow 1987), and has recently been anby the unavailabilityof cladisticanalysesof avi- alyzed for a large and diversegroup of birds
an character data, with which the behavioral
(McKitrick 1991). The latter data set was chosen
data could be either comparedor combined to
generatea detailed hypothesisabout the evolution of parental care in birds. Furthermore,
to complementthe behavioraldatasummarized
here becauseit is the most taxonomicallycomprehensiveset of characterdata available for
830
MiddyC. MCKIT•CK
birds. No assumptionsare made here about the
independence
of the hindlimbmusculature
and
parental-carebehavior.
I used published data on 66 charactersfrom arian
hindlimb musculature(for details,seeMcKitrick 1991),
these with
taken from the literature.
The behaviors
were chosen
are present in 75% of all trees. It was chosenover the
Completeor interpretablebehavioraldatawere not
alwaysavailablefor the sametaxausedby McKitrick
(1991). Therefore, in 13 casesa speciesclassifiedin
the same genus was substituted(see Appendix 2).
characters were obtained
An ancestor based on crocodilians
for 76 arian taxa.
was used as the
outgroup."Dummy" charactersfor paleognath(ratites and tinamous), neognath (all other birds), and
arian monophylywere includedaswell. Thesehelped
to ensure that the outgroup would always remain
outsideof the ingroup (for justification,seeMcKitrick
1991). Furthermore,the analyseswere constrained
(usinga "opological Constraints"option in program
used;seebelow) suchthat paleognathswere the sister
groupto neognaths.Thus,the paleognathswere designated as the sistergroup to neognaths,and the Ancestorwasincludedasthe sistergroup to all the birds.
This structureis the basisfor outgroup comparison
(Ralkow 1982,Maddison et al. 1984)and permits one
to test hypothesesof synapomorphy;if a character
state is synapomorphousfor the ingroup, then the
two outgroups(in this casethe "sister group" and
outgroup) should have the alternative characterstate.
The combineddata set was analyzed using PAUP
3.0s(PhylogeneticAnalysisUsing Parsimony;Swofford 1990) on a Macintosh IIfx computer.The hindlimb characters
alsowere analyzedseparatelyto determine whether the behavioral charactersactually
were makinga differencein the resultingtreetopology. The Heuristic algorithm was used,asit finds the
minimum length treesand is recommendedfor data
more than 20 taxa. The shortest trees were
found usingthe RandomAddition option becausethe
order in which the taxaare read by the programcan
make a significantdifferencein whether the shortest
tree is found. With this option, the taxa are read in
random order 10 different times, and for each replication I allowed a maximumof 50 trees to be generated.I then took one of the resulting shortesttrees
and usedthisasa "seed"to completethe analysis(i.e.
from thisseedall possibleminimum-lengthtreeswere
sought).Initial analysisproduceda numberof groups
that were consideredby PAUP to be "the same";in
other words, these groups contained three or more
taxa at the same node. In order
60.
A 75%majority-ruleconsensus
of the final treeswas
obtained(Fig. 1);sucha treeshowsall groupingsthat
describedbriefly in Appendix 1.
sets with
pothesesabout character evolution, I examined each
characters
15 behavioral
becausethey summarizeparental care in birds and
becausethey seemedamenableto relatively unambiguousinterpretationand coding.All charactersare
Behavioral
number of treesand thereby reducethe number of
assumptions
that were necessaryfor formulatinghy-
of thesegroupsof "same"taxaand arbitrarilyeliminated all but one of the taxa in each group. This
resultedin eliminationof 17 taxa,leavinga total of
METHODS
and combined
[Auk,Vol. 109
to reduce
the final
strict-consensus
tree becausethe latter collapsesall
groupingsthat do not occur in 100%of the trees. I
considerthe majority-rule tree to be a more representativeand informative summaryof relationships.
Becausethe consensustree is a summary, rather
than an actual hypothesisof charactertransitions,I
used one of the actual shortest-lengthtrees (Fig. 2;
designated Tree 1) to illustrate these transitions. Of
58 nodesin the consensus
tree (Fig. 1), only four
(6.9%) were unstable; this indicates that all of the
fundamental(actual)treeswere generallyvery similar. For this reason,using one tree to representall
of the treesis a usefulway to illustratepossiblecharacter transitions. Three optimization routines were
applied to Tree 1 (Acctran, Deltran, and MinF; see
below). Theseoptimizationsare different methodsof
assigningcharacterstatesto the interior nodes(hypotheticalancestors)
of the treesgeneratedby PAUP.
For example,in Figure 2 the terminal taxa Rheaand
Crypturellus
are linked at node 61. For somecharacters,
there is a transition of character states between node
62 and node 61, and between node 61 and Rhea. The
three optimizationroutinesalwayswill yield trees
with the sameoverall number of transitions(steps),
but the transitions between nodes 62 and 61, and
between
node 61 and Rhea will
not be the same for
each optimization. The Acctran (Accelerated Transformation)algorithm is basedon the assumptionthat
reversals (0 • 1 • 0) are more common than independent origins of a characterstate(1 • 0 • 1), while
Deltran (Delayed Transformation)assumesthe opposite (i.e. independentorigins are more common
than reversals). The MinF routine maximizes the
numberof autapomorphies(derivedstatesunique to
that terminal taxon) wherever possible.Therefore,
the algorithmsmakedifferentassumptions
aboutevolutionary processes.
Severalof the charactersused in this analysisare
relatively unenlighteningbecauselittle information
is available about them in the literature. Nevertheless,
I included such characters to call attention to the lack
of information.One suchexampleis mateguarding
by males(character72).In mostcases,
the information
is simply unavailable(seeBirkhead1979);in others,
the author mayhaveobservedmateguardingbut did
not mention it, or was not explicit about whether it
occurs.For example, Mock (1979) noted that males
are very stronglyterritorial during the egg-laying
stage in Ardea herodias;however, he did not refer to
October1992]
Phylogeny
ofAvianParental
Care
831
Ancestor
Rhea
Ancestor
Rhea
•-E•
crypturellus
•
Nothoprocta
--
t;2
.['61
C Nothoprocta
Crypturellus
--
Dapt•n
Daption
Oceanires
Oceanires
Fregotta
--
Oceanodroma
--
Ocean•droma
Pygoscelis
Eudyptula
Eudyptula
Gayla
r8c Gavia
Pcdiceps
--
Chen
Chen
Copphus
]
•
•
•
Cororhinca
__•
Cepphus
Ptychoramphu$
ß76•'- Fratercula
Cororhinca
Rynchops
r•
Rynchops
8o 79-[• Stoma
L
Larus
Stercoranus
118
Grus
Fulica
-8? E Gymnogyps
Coragyps
Gymnogyps
Mycteria
[-91•
Ciconia
•
Plegadis
5
Florida
.96½
½ Butoride
Acc•iter
113
•
..•?.•
103
--
[111J 107J
/I
06%
1
I
'
I
'
I
r-- coccyzus
{ G•coccyx
Eulampls
,lo4r--Colaptos
I
]
Acc•iter
'-•
Co•,us
I10•,n•---- Geococcyx
[ E o•xu•a
Fig. 1. A 75%majority-ruleconsensus
of 63 trees
based on hindlimb
muscle and behavioral data; all
Fig.2. Tree 1 of 63 basedon hindlimb muscleand
behavioral
data. Internal
nodes are numbered.
groups occurred in 100% of these trees unless otherwise
indicated.
thisbehaviorasmateguardingand,therefore,I coded
that characterwith "?" (missing)for that species.
A growing number of apparently monogamous
specieshave been shown to exhibit multiple parentagein their broods(for a review, seeMcKitrick 1990).
Unfortunately, little information on actualparentage
is available for most of the primarily nonpasserine
speciesincluded in the presentanalysis.Extra-pair
copulationshave been reported in several of these
species(seeGladstone1979,Ford 1983).Becausethe
speciesexhibitingthe behaviorappeartobe primarily
monogamous,
I havecodedspeciesshowingmultiple
parentageor extra-pair copulationsas "0" (monogamous) for character 70.
Character75 (defenseof young/parentalcare)is in
effecta summaryof parental carein birds. Generally,
if a specieswasbiparentalfor other aspectsof careit
wasbiparentalfor character75 aswell. Occasionally,
however, a specieshad female-only care in most respects,but malescontributeddefense.In thesecases,
character75 wascodedasbiparental,while the other
care-relatedcharacterswere codedas female-only.
Character 76 (distinguishablereversed sexual dimorphism)wascodedin a nontraditionalmannerfor
owls. Although owls are consideredto exhibit reversedsexualdimorphism(Mueller 1986),I did not
so code the two owls included in this analysis.The
ratio of male wing length to femalewing length is
0.975in Otusasioand 0.952in Bubovirginianus
(Mueller
1986:table 1); these numbers are so close to 1.000 that
classifyingthesespeciesas showingreversedsexual
dimorphism seemed unwarranted.
Character84 (posthatching
development)wascoded
basedon the classification
systemof Winklet and Walters (1983),but their three categoriesof precociality
were lumpedinto one, as were their two categories
of altriciality.Taxawhoseclassification
wasspeculative were codedashaving that speculativecondition.
832
MARYC. MCKITRICK
Ancestor
Rhea
[Auk, Vol. 109
hypothesizedcharactertransitionsdescribedin
F CryptttrellusAppendix 3 are basedon this tree.
--
Ocean•droma
Fregetta
Eudyptula
Gayla
--
]
L-•
•
•
For the analysesbasedon hindlimb dataonly,
161 trees of 247 stepswere found (consistency
index excluding uninformative characterswas
0.357). A 75% majority-rule consensusof these
trees is shown in Figure 3.
then
Alca
DISCUSSION
Uria
Brachyramphus
Cepphus
Ptychoramphus
Cetorhinca
The consistencyindices are higher than expectedfor this number of taxa (consistencyinRynchop$
dex of 0.30 expectedfor 60 taxa; the expected
•
Stema
value decreases
with increasingnumbersof taxa
basedon empirical analysisby Sandersonand
Ardea
Butorioles
Donoghue 1989). The level of homoplasy,
FIodda
therefore, is not high for a data set of this size.
•
Coragyps
•
Gymnogyps
However, many nontraditionalgroupsappear
Grus
Fulica
in theseanalysescomparedwith the topology
r•__[• Lepfopt#os
Mycteria of the treesobtainedby McKitrick (1991) using
r-•
I
Ciconia
•
Phoeniconwushindlimb muscle data for a larger number of
taxa. For example,whereasauks are monophyDendragapus
letic and gulls and terns are as well, the two
Falco
groups do not cluster together. Auks (Fig. 2,
node 77) cluster with procellariiforms, penChaetura
guins, loonsand grebes(node 71). The results
Eulampis
of the analysisof morphologyplus behaviorare
Tyrannus
very similar to thosefrom the analysisof morChordeiles
phologyalone,differingprimarily in the placeCoccyzus
ment of grouse,ducks,herons,and the hoatzin.
Geococcyx
CrotOphaga
Zenaida
This suggests
that neither datasetis biasingthe
Opisthocomus
resultsunduly, and that both data setscontain
Fig. 3. A 75%maiority-ruleconsensus
tree of 161 a comparabledegreeof historicalinformation.
treesbasedon hindlimb muscledata only; all groups
I suggestthat the present results can be reoccurred in 100% of these trees unless otherwise ingardedasa startingpoint, an exerciseillustratdicated.
ing how comparativephylogeneticdatamay be
'
•
Fratercula
• -89%
Cathartes
• ccpiter
employedto understandthe evolutionof charSeeAppendix 1 for a completelist of charactersused
in the analysis.The characterdata are shown in Appendix 2.
RESULTS
acter suites(such as behaviorsinvolved in parental care).As more data becomeavailable, the
resultsof suchanalyseswill be more representative of the true phylogeny and of character
evolution
as well.
The resultsof suchanalysesmay be appraised
I found 63 shortest-lengthtreesof 339 steps from two perspectives.The trees may be conbased on muscle and behavioral data; the considered as hypothesesabout the phylogenetic
sistencyindex (ci) excluding uninformative relationshipsamong the taxa under considercharacters was 0.353. Uninformative
characters
ation. The trees also may be consideredas hyare those that show only one transition at a pothesesabout the evolution of the characters
terminal taxon (i.e. they are autapomorphies). themselves,although someauthorswould disA 75% majority-rule consensustree, showing agree(e.g. Brooksand McLennan 1991:63,1991:
the percentageof the 63 treesin which each 141).Thesehypothesesare constrainedby one's
group appears,is depictedin Figure 1. Figure starting assumptions,namely, that ratites are
2 shows the first of the 63 trees (Tree 1); the
the sistergroup to neognathsand crocodilians
October
1992]
Phylogeny
ofArianParental
Care
arethe sistergroupto birds.Appendix3 shows
the hypothesizedchangesin the behavioral
charactersusing three optimization routines.
The hypotheses
are basedon Tree 1 of 63. A
few of these are described below.
833
Accordingto Acctran,female-onlycare(state0)
isprimitivefor birds,with biparentalcare(state
1) arisingnear the baseof the avian lineage,at
node 113 (neognathsminus the duck-grouse
group).Thereisonetransitionto male-onlycare,
For character70 (mating system),monogamy in ratites,and one reversalto female-only care,
With Deltran, no-careis primitive
(state0) is primitive within birds (as has been in Eulampis.
generallyassumed)
when Acctranis used;Del- for birds, with a transition to biparental careat
tran and MinF show polygyny (state1) at the node 113,one to male-only carein ratites,and
baseof the avian lineage with a transition to two to female-only care, in the duck-grouse
With MinF, biparental
monogamyoccurringnear the basalnode (at groupand in Eulampis.
node 117,with only ratitesexcludedfrom this careis primitive, and male-onlycarearisesin
clade). Acctran shows three independent ori- ratites, while female-only care arisesin the
ginsof polygyny,while MinF showsone. All duck-grousegroup and in Eulampis.
For character81 (postfledgingcare), all opoptimizationsshowtwo independentoriginsof
timizationsyield identicalhypotheses.
Biparenpromiscuity(state3).
Character75 (defenseof young/parentalcare) tal care (state 1) is primitive within birds. In
is of particularinterest,as it summarizesthe addition, there is one transition to female-only
roles of the sexesin caring for the young. All care (at the duck-grouseclade), two to malethree optimizationsindicatethat someform of only care(at nodes62, 73 and in Zenaida),and
biparentalcare(defenseof young)is primitive three to no-care (at node 78 and in Florida and
for birds.
Character transitions for character 78 (incu-
Chaetura).
lineage (between nodes 117 and 113). Femaleonly incubation occursin the lineage at node
116, the duck-galliform clade. Biparental incubation (state 1) is a synapomorphy(shared-
For character82 (group breeding), state 1 of
character82 has arisen unambiguouslythree
times (in Chaetura,Corvus,and Crotophaga).
For character84 (posthatchingdevelopment),
all transitionsare unambiguous.Precocialityis
primitive (state0), and altriciality (state1) arose
in the large clade (node 113) that containsall
birds exceptducks,grouse,the hoatzin, and ratites. Altriciality was subsequentlylost three
derived character state) for the remainder of the
times: at node 85, and in Phoeniconaiusand Chor-
neognaths(seeMethods) and, therefore, primitive within this group. Male-only incubation
deiles.
(state 2) arises once, at the base of the ratite
analysisto determinewhich ecologicaland lifehistory parameterswere the best predictorsof
bation) are complex. According to Acctran, a
transition from no incubation (state 3; croco-
dilians do not incubate) to female-only incubation (state 0) occurs at the base of the avian
lineage (node 62). In all, female-only incubation arises four times. Deltran represents noincubationasbeing the primitive condition for
birds and, thus, female-only incubation is derived for the duck-galliform clade rather than
primitive. Biparental incubation is a synapomorphy for the remainder of the neognaths,
and male-only incubation is a synapomorphy
for the ratites.Female-onlycarearisesa total of
six times. Finally, MinF representsbiparental
incubation as a synapomorphyfor birds and,
thus,it is primitive within that lineage.Again,
female-onlyincubationis derived for the duckgalliform lineage,and for five other lineagesas
well. Male-only incubationis derived for rat-
Silver et al. (1985) used canonical-correlation
various aspectsof avian paternal care. Their resuits indicated that mode of posthatching development, mating system,some habitat characteristics,and relative clutch massexplain the
mostvariancein paternal-careactivities.I used
the phylogenetic framework of the present
analysisto test the hypothesisof Silver et al.
(1985)that the evolutionof paternalcareis causally correlatedwith the occurrenceof altriciality.
The more data that becomeavailable for phylogeneticanalysis,the more ways we can invent
for studying characterevolution; unfortunate-
ly, the invention of algorithmsfor testing hypothesesabout characterevolution necessarily
For character80 (posthatchingcare),the three lagsbehind. At present,no algorithmsare availoptimizationseachleadto differenthypotheses. able for testing significanceof associationbeites.
834
MARY
C. MCKITRICK
[Auk,Vol.109
I examinedthe distribution of statechangesin
character80 (posthatchingcare)with respectto
the occurrenceof an independent character(see
below), and receded the character as presence
or absenceof paternal care. For example, "biparental care" became "paternal care present";
"female-only care" became "paternal care absent." The origin of female-only or no parental
care subsequentto the origin of biparental or
male-only care was interpreted as a lossof paternal care. Figure 4 shows the state changes
for character80 beforereceding;Figure 5 shows
the receded
transitions
for this character.
Of the predictorsstudiedby Silveret al. (1985),
posthatchingdevelopment and mating system
were the only ones analyzed in the present
study.Of thesetwo, posthatchingdevelopment
wasthe only one for which hypothesizedcharactertransitionswere identical for all three eptimizatiens
Colapres
on Tree
1. I traced
the
occurrence
of the derived state of this character,namely
altriciality, onto that tree (Figs. 4 and 5). Its
occurrence
is referred
to as the black area of the
tree. To testthe hypothesisof Silver et al. (1985),
I wished to determine the probability of obtaining as many or more gains in the black and
as many or fewer lossesin the black simply by
Fig. 4. Tree 1 showing occurrenceof altriciality
(heavyblacklines)and statetransitionsfor character chance. In other words, does the black area at80 (posthatchingcare of young).
tract gains and repel losses?Should the occur-
renceof altricialityleadto the origin of paternal
tween multistate characters. Maddison (1990)
presented an algorithm to test associationbetween binary characters;that is, to determine
the likelihood of an observednumber of gains
and lossesin a "dependent" variable occurring
by chancewith respectto the occurrenceof an
independentvariable. This test is designednot
to study correlation of change in one variable
with changein another, asother methodshave
done (e.g. Felsenstein1985),but rather to test
the significanceof the origin of the dependent
variable anywhere subsequentto the origin(s)
of the independentvariable on the tree. In other words, it teststhe null hypothesisthat gains
and lossesof the dependent characterare randomly distributed on the tree with respectto
the state of the independent character. This
makesthe test ideal for studying evolutionary
causalityin correlationsamongcharacterstates.
Maddisen (1990) suggestedways to recede
multistate charactersas binary charactersfor
purposesof this test,and he further pointed out
that the testis probablymoreconservativewhen
the characters tested were used to build the trees.
care in character 80? The observed pattern of
gainsand lossesin the blackareawas zero gains
and one loss (Fig. 5), and the probability of
obtaining this pattern by chance is 0.814. In
other words, the pattern is not significant and
altriciality doesnot appearto lead to the origin
of paternal care.The implicit assumptionof Silver et al. (1985) was that female-only care is
primitive for birds, whereas in fact biparental
care is primitive (and widespread;Fig. 4). Evidently, factorsother than altriciality were the
selectiveagent for the origin of paternal care
in birds.
Emlen and Oring (1977) hypothesized that
"complete male parental care" (which ! interpret to mean male-only care)arosein taxawith
a shared history of incubation. To examine this
hypothesis,I mapped onto Tree 1 the occurrence of shared incubation (character78), as indicated by Acctran optimization (Fig. 6), and
the origin of male-only care for character 81
(pestfledgingcare). The map shows an early
origin of sharedincubation within birds, with
four out of five originsof male-only carearising
October
1992]
Phylogeny
ofAvianParental
Care
835
A•stor
Rhea
NothO•octa
Cha•ura
CHARACTER 80 RECODED
Fig. 5. Tree 1 showing character80 recoded.
in taxawith a history of sharedincubation.One
origin of male-only care occurred in a group
(ratites)with no history of parental incubation.
Thus,Emlen and Oring's (1977)hypothesisappearsto be largely supported.However, Maddison's(1990) testindicatesthat the probability
of obtaining four or more gains in the black
area is 0.757. This is partly due to the fact that
sharedincubationis so widely distributed on
the tree. A higher representationof members
of Passeriformes
in the tree might well change
this result, as many passerinesdo not have
shared incubation.
Basedon the datapresentedhere,van Rhijn's
(1990) hypothesisthat male-only parentalcare
is primitive within birds is incorrect. I believe
Fig. 6. Tree 1 showing origin and loss of shared
incubationand origin and lossof male-only care for
character81 (postfledgingcare).
pothesesbased on phylogeneticanalysisof
characterdata and then examinethe possible
evolutionarypathwaysrevealed by the data.
Furthermore,separatingparental-carebehavior
into component parts is more useful than examining parental care as a unit, as separation
revealsthe decouplingof someaspectsof care.
For example,careof nestlingsmay be biparental, while care of fledglingsis uniparental,as
in some auks.
Drawbacksof the phylogenetic
analysis.--Several problemsare inherent in a study of this
kind. Immelmann (1974) noted that certain
kinds of behavioral
characters are not "taxo-
that van Rhijn's approachhas merit in that it nomically"usefulbecause
of their plasticityin
attemptsto place the study of behavioral evo- responseto environmental variables. However,
lution within a phylogeneticframework,where hypothesesof convergencecan only be made
it belongs.However, his proposalsregarding within the contextof a phylogenetichypothethe direction of evolution
are ad hoc in that
sis;in otherwords,onecannotdetermineapriori
they are ahistorical,are made outsidethe con- whether a given characterwill be phylogenettext of an explicit phylogenetichypothesis,and icallyinformative.The meanconsistency
index
are basedon somenotion of probability and the was not significantly different for the muscle
irreversibility of certain evolutionary path- characters(0.542) and the behavioral characters
ways. It is more meaningful to formulate hy- (0.420; Kruskal-Wallis, k = 1.095, df = 1, P =
836
MARYC. MCKITRICK
0.295), suggestingthat the two kinds of charactershave equal potential to be phylogenetically informative.
Throughphylogeneticanalysisone may learn
[Auk,Vol. 109
for future researchon avian mating systems.
One of thesewas to askwhy malesin monogamoussystemscontributesomuchparentalcare.
My analysismakesit possibleto begin to try to
more about the tendencies of certain characters
answersucha question.For example,if we know
to originate in many taxa. Even if a character how many times male-only postfiedging care
exhibits homoplasy,however, it still may be arosefrom biparentalcare,and how many times
informative at some lower taxonomic level. If,
the absenceof postfiedgingcare arose,we can
however, these environmental variables cause makecomparisons
of ecologicalvariation across
intraindividual variation in parental-care be- taxaand form useful hypothesesaboutthe conhavior, which they undoubtedlydo (Emlen and ditionsleadingto the evolution of suchpatterns
Oring ! 977),then the classificationof behaviors of care.
usedin the presentstudy is probablysomewhat
Although my study is to date the mosttaxoinaccurate.
nomically comprehensiveattempt to analyze
The classificationof behaviormay be complex phylogeneticallyavian parental-caredata, it is
(Shields 1984), and the classificationof mating neverthelesslimited in its scopeby the availsystemsin particular can be cumbersome(Or- ability of information. Of great interest, for exing 1982, Mock 1983). Consequently,coding ample, would be a cladisticanalysisof the Chacharactersmay fail to characterizethe behaviors radriiformes, a group within which parentaladequately, even though much attention was care behavior varies widely. At present there
paid to this in the present analysis. Further- are no comparabledata on the limb musculature
more, even though both sexesmay perform a for the majority of this group, in particular the
certain carebehavior, there may be quantitative sandpipers(Scolopacidae),so very few repreor qualitative differencesin the care provided sentatives of the order are included here. Morby each (Winkler 1987);this is not reflectedin phologicalwork on that group is in progress
the presentqualitativecodingsystem.There may (McKitrick unpubl. data, P. Chu unpubl. data)
be intraspecificgeographic variation in paren- and, eventually, these data will be combined
tal care (e.g. Agelaiusphoeniceus;
Payne 1969, with behavioraldatafor a detailedphylogenetic
1979) that is not accountedfor in the present analysis.Also, few passerinespecieswere incoding scheme.
cluded in the current analysis,despite the inFor at least two reasons,I have attempted to terestingvariation in their parental-carebehavbe conservative in my interpretation of hy- ior, because their hindlimb musculature is
pothesesyielded by the phylogeneticanalyses relatively uninformative phylogenetically(e.g.
in this study. One reasonis that some of the Raikow 1978, McKitrick ! 985). For the charadriphylogenetic relationshipssuggestedby these iforms and passetines,the behavioral data base
analysesdiffer markedly from all others pro- is richer than the morphologicalone.Collecting
posed in the literature, including those based the original data is a painstaking process;colon the same data but with more taxa included
lating the data from the published literature is
(McKitrick 1991). If the relationships as pre- fraught with difficulties,such as the danger of
sented here are incorrect, as at least some unmaking errorsin interpreting the work of many
doubtedly are, then the hypothesesabout char- different researcherswho have brought differacter transformations
are also incorrect. g second
ent methods, assumptions,and biasesto their
reason, related to the first, is that the addition
work. Furthermore,a morphologistis likely at
or deletion
of characters and taxa has an imtimes to misinterpret behavioral studies.
Brooks and McLennan (1991:342) noted that
portant effect on tree topology and, as more
information
becomes available for the taxa ex"We have discoveredthat there is a paucity of
amined in this study or subsetsof these taxa, rigorousphylogenetic hypothesesfrom which
more meaningful statements about character we can begin historicalecologicalstudies.... "
This is an extreme understatement, and in exevolution will be possible.
A phylogenetic approachcan yield hypoth- pressing it the authors might well have menesesabout the pattern of origin of behavioral tioned alsothe paucity of comparativedata sets
characters, so that the appropriate kinds of for the same group of taxa. What I have prequestionscan be asked about these patterns. sented here is an attempt to begin to remedy
Mock (1985) suggestedseverallines of inquiry this for birds. I am optimistic that future work-
October
1992]
Phylogeny
ofAvianParental
Care
ers will continue to gather anatomical, behavioral and other "phenotypic" data (including
molecular) for a wide variety of taxa. It is my
hope that these workers will gather such data
with the goal of using them for analyseslike
the present one, analysesthat will be greater
both in scopeand in detail. Through suchwork
we have an excellent chanceof formulating rigoroushypothesesabout phylogenetic relationships among birds and about the evolution of
complexavian charactersystems.
ACKNOWLEDGMENTS
I thank Philip Chu and William Fink for much
helpful discussionof phylogeneticanalysis,and Phil
Myers for advice on statistics.Steve Beissinger,Phil
Chu, Raymond Pierotti, Gary Schnell, Sarah Sloane,
David Winklet, and an anonymous reviewer criticized earlier drafts of the manuscriptand provided
many useful suggestions.Wayne Maddison generously assistedwith application of his correlation test.
Robert Storer provided information on grebes,Raymond Pierottiprovidedinformationon gullsand auks,
and Cynthia Simsprovidedreferenceson Corvus.This
work was supportedby grant BSR-9006208from the
National
Science
Foundation.
837
the Common Murre Uria aalge.Anim. Behav.33:
608-619.
BIRKHEAD,
T. R., AND C. M. LESSELLS.
1988. Copulation behaviour of the Osprey Pandionhaliaetus.
Anim.
Behav.
36:1672-1682.
BJ•RKLUND,
M. 1990. A phylogeneticinterpretation
of sexualdimorphismin body sizeand ornament
in relation to mating systemin birds. J.Evol. Biol.
3:171-183.
BOSWALL,
J., ANDD. MAClvER. 1975. The Magellanic
PenguinSpheniscus
magellanicus.
Pages271-305 in
The biology of penguins (B. Stonehouse,Ed.).
University Park Press,Baltimore.
BROOKS,
D. R., •3'•DD. A. MCLENN•3'•. 1991. Phylogeny, ecology, and behavior: A researchprogram
in comparative biology. Univ. Chicago Press,
Chicago.
BROWN,L. H., AND A. ROOT. 1971. The breeding
behaviour of the LesserFlamingo Phoeniconaius
minor. Ibis 113:147-172.
BRUNING,D. F. 1974. Socialstructureand reproductive behavior in the Greater Rhea. Living Bird
13:251-294.
BURGER,
J. 1981. Sexual differences in parental activities of breeding Black Skimmers. Am. Nat.
117:975-984.
BURGER,J., L. M. MILLER, AND D.C.
HAHN.
1978.
Behavior and sex roles of nesting Anhingas at
San Bias, Mexico. Wilson Bull. 90:359-375.
LITERATURE CITED
AINLEY, D. G., R. E. LERESCHE,AND W. J. L. SLADEN.
1983. Breedingbiology of the Ad•lie Penguin.
Univ. California Press,Berkeley.
AINLEY, D. G., AND g. P. SCHLATTER. 1972.
Chick-
raising ability in Ad•lie Penguins.Auk 89:559566.
ALLEN,A.A. 1924. A contributionto the life history
and economic status of the Screech Owl (Otus
asio). Auk 41:1-16.
ASHCROFT,
R. 1979. Survival ratesand breeding biology of Puffins on Skomer Island, Wales. Ornis
Scand. 10:100-110.
BAYNARD,
O.E. 1913. Home life of the GlossyIbis
(Plegadisautumnolis
Linn.). Wilson Bull. 25:103-
BURNS,F.L. 1900. A monograph of the Flicker (Colaptesauratus).Wilson Bull. 12:1-82.
BUTLER,R. G., AND S. JANES-BUTLER.
1983. Sexual
differences
in the behavior
of adult Great Black-
backed Gulls (Larusmarinus)during the pre- and
post-hatchingperiods.Auk 100:63-75.
CLUTTON-BROCK,T. H., AND P. H. HARVEY. 1977. Pri-
mate ecology and social organization. J. Zool.
(Lond.) 183:1-33.
CLUTTON-BROCK, T. H., AND P. H. HARVEY.
1979.
Comparisonand adaptation. Proc. R. Soc. Lond.
Set. B Biol.
Sci. 205:547-565.
CODDINGTON,
J. g. 1988. Cladistic tests of adaptational hypotheses.Cladistics4:3-22.
COLES,V. 1944. Nesting of the Turkey Vulture in
Ohio
caves. Auk
61:219-228.
COOKE, F., M. A. BOUSFIELD,AND A. SADURA. 1981.
117.
BECK,J. R., AND D. W. BROWN. 1971. The breeding
biologyof the Black-belliedStorm-PetrelFregetta
Mate change and reproductive successin the
Lesser Snow Goose. Condor
83:322-327.
CRACRAET,
J. 1981. Toward a phylogenetic classifi-
tropica.Ibis 113:73-90.
BENT, A. C. 1940. Life histories of North American
cuckoos,goatsuckers,
hummingbirdsand their
cation of the Recent birds of the world (class
Aves). Auk 98:681-714.
CRACRA•T,
J. 1986. The origin and early diversification of birds. Paleobiology 12:383-399.
J. AND D. P. MINDELL. 1989. The early
the White-fronted Amazon (Amazonaalbifrons, CRACRAFT,
Psittaciformes). Auk 101:74-92.
history of modern birds: A comparisonof molecularand morphologicalevidence.Pages389BIRKHEAD,
T.R. 1979. Mate-guarding in the Magpie
Pica pica.Anim. Behav. 27:866-874.
403 in The hierarchyof life (B. Fernholm,K. BreBIRKHEAD,T. R., S. D. JOHNSON,AND D. N. NETTLESHIP.
met and H. J6rnvall, Eds.). Elsevier SciencePublishers, Amsterdam.
1985. Extra-pair matings and mate guarding in
allies. U.S. Natl.
BERMAN, S.L.
Mus. Bull.
176.
1984. The hindlimb musculature of
838
MARYC. McKITRICK
DALKE, P. D., A. S. LEOPOLD, AND D. L. SPENCER. 1946.
The ecologyand managementof the Wild Turkey
in Missouri. Conserv. Comm., Federal Aid-Wild-
life Prog.,Tech.Bull. No. 1.
DERKSON,
D.V. 1977. A quantitativeanalysisof the
incubationbehaviorof the Ad•lie Penguin.Auk
94:552-566.
DEXTER,R. W. 1952. Extra-parental cooperation in
the nestingof Chimney Swifts. Wilson Bull. 64:
133-139.
DEXTER,
R. W. 1961. Further studieson nestingof
the Common Nighthawk. Bird-Banding32:7985.
[Auk,Vol. 109
HARRIS,M.P. 1966. Breeding biology of the Manx
ShearwaterPuffinuspuffinus.Ibis 108:17-33.
HARRIS,M.P., ANDT. R. BIRKHEAD.1985. Breeding
ecologyof the Atlantic Alcidae.Pages156-204in
The Atlantic Alcidae (D. N. Nettleship and T. R.
Birkhead, Eds.). Academic Press,London.
HARVEY,P. H., ANDG. M. MACE. 1982. Comparisons
between taxa and adaptive trends: Problems of
methodology.Pages343-361 in Current problems in sociobiology(King's College Sociobiology Group, Eds.). Cambridge Univ. Press,Cambridge.
HATCH,S. A. 1987. Adult survival and productivity
of Northern
Fulmars in Alaska. Condor 89:685DOBSON,F. S. 1985. The use of phylogeny in be696.
havior and ecology.Evolution39:1384-1388.
DRENT,R.H. 1965. Breedingbiology of the Pigeon HATCH, S.A. 1990. Individual variation in behavior
Guillemot, Cepphus
columba.
Ardea 53:99-160.
and breedingsuccess
of Northern Fulmars.Auk
107:750-755.
ELLISON,
L.N. 1973. Seasonalsocialorganizationand
B.J. 1988. Intraspecificvariation in exmovements of Spruce Grouse. Condor 75:375- HATCHWELL,
385.
tra-paircopulationand matedefencein Common
Guillemots Uria aalge.Behaviour 107:157-185.
EMLEN,
S. T., ANDL. W. ORING.1977. Ecology,sexual
selection,and the evolution of mating systems. HAVERSCHMIDT,F. 1949. The life of the White Stork.
Science
197:215-223.
ERPaNGTON,P. L.
E. J. Brill, Leiden.
1932. Studies on the behavior of
HODGEs,
A.F. 1969. A time lapsestudy of Kittiwake
the Great Horned Owl. Wilson Bull. 44:212-220.
incubationrhythms.Ibis 111:442-443.
FELSENSTEIN,
J. 1985. Phylogeniesand the compar- HOGLUND,J. 1989. Size and plumage dimorphism
ative method. Am. Nat. 125:1-15.
in lek-breeding birds: A comparativeanalysis.
Am. Nat. 134:72-87.
FINNEY,G. H., AND F. COOKE. 1978. Reproductive
habits in the Snow Goose: The influence
of fe-
male age. Condor80:147-158.
FISCHER,
R. B. 1958. The breeding biology of the
Chimney Swift, Chaetura
pelagica
(Linnaeus).N.Y.
State Mus. Sci. Serv. Bull. 368:1-141.
FISHER,
H. I. 1971. The LaysanAlbatross:Its incubation, hatching,and associatedbehaviors.Living Bird 10:19-78.
HUNT, R.H.
1975. Maternal behavior in the More-
let's crocodile, Crocodylusmoreleti.Copeia 1975:
763-764.
IMBER,M. J. 1987. Breedingecologyand conservation of the BlackPetrel (Procellaria
parkinsoni).
Notornis
34:19-39.
IMMELMANN, K. 1974. The use of behavioural char-
acters in avian classification.Page 206 in Proceedings16th InternationalOrnithologicalConBehavior and food habits of the Red-tailed Hawk.
gress(H. J.Frith and J.H. Calaby,Eds.).Canberra,
Condor 48:205-237.
1974.Australian Academyof Science,Canberra.
FOLSE,
L. J.,JR.,ANDK. A. ARNOLD.1978. Population JOHNSGARD,
P. A. 1961. The taxonomy of the Anatecologyof Roadrunners(Geococcyx
californianus)
idae--A behaviouralanalysis.Ibis 103a:71-85.
in South Texas. Southwest. Nat. 23:1-28.
JOHNSON,
R. A. 1941. Nesting behavior of the AtFORD,N.L. 1983. Variation in mate fidelity in molantic Murre. Auk 58:153-163.
nogamousbirds. Curr. Ornithol. 1:329-356.
JOYNER,
D.E. 1977. Behaviorof Ruddy Duck broods
GEORGE,
J. C., ANDA. J. BURGER.1966. Avian myolin Utah. Auk 94:343-349.
ogy. AcademicPress,New York.
KAHL,M.P. 1966. A contributionto the ecologyand
GITTLEMAN,
J. L. 1981. The phylogeny of parental
reproductivebiologyof the MarabouStork (Lepcare in fishes. Anita. Behav. 29:936-941.
FITCH, H. S., F. SWENSON,AND D. F. TILLOTSON. 1946.
GLADFELTER,
H. L., AND R. S. McBuP,NEY. 1971. Mat-
ing activityof RuffedGrouse.Auk 88:176-177.
GLADSTONE,
D.E. 1979. Promiscuityin monogamous
colonial
birds. Am. Nat. 114:545-557.
GooD, E. E. 1952. The life history of the American
Crow (Corvusbrachyrhynchos
Brehm). Ph.D. dissertation, Ohio State Univ., Columbus.
GOODBURN,
S.F. 1984. Mateguardingin the Mallard
Anasplatyrhynchos.
Ornis Scand.15:261-265.
GREEN,
R. 1976. Breedingbehaviourof OspreysPandion haliaetus in Scotland. Ibis 118:475-490.
toptilos
crumeniferos)
in EastAfrica.J.Zool.(Lond.)
148:289-311.
KAHL,M.P. 1972. Comparativeethologyof the Ciconiidae.The woodstorks
(generaMycteriaand Ibis).
Ibis 114:15-29.
KEITH, L. B. 1977. Great Horned Owl. Can. Wildl.
Serv. Dep. Supply & Services,Ottawa.
KILHAM, L. 1966. Reproductive behavior of Hairy
Woodpeckers.I. Pair formation and courtship.
Wilson
Bull. 78:251-265.
KILHAM,L. 1968. Reproductivebehavior of Hairy
October
1992]
Phylogeny
ofAvianParental
Care
Woodpeckers.
II. Nestingand habitat.WilsonBull.
80:286-305.
KILHAM,L. 1969. Reproductivebehavior of Hairy
Woodpeckers.III. Agonisticbehavior in relation
to courtship and territory. Wilson Bull. 81:169183.
839
comparativeethology and phylogeneticsystematics:A casestudy using gasterosteidfishes.Can.
J. Zool. 66:2177-2190.
MOCK,D.W. 1979. Displayand repertoireshiftsand
"extra-marital" courtship in herons. Behaviour
69:57-71.
MOCK,D. W. 1983. On the study of avian mating
in birds. Methuen & Co., London.
systems.Pages55-84 in Perspectives
in ornitholLANCASTER,
D.A. 1964. Life historyof the Boucard
ogy (A. H. Brushand G. A. Clark, Eds.).Cambridge Univ. Press,Cambridge.
Tinamou in British Honduras Part II: Breeding
biology. Condor 66:253-276.
MOCK,D.W. 1985. An introductionto the neglected
LANK, D. B., P. MINEAU, R. F. ROCKWELL,
AND F. COOKE.
mating system.Pages 1-10 in Avian monogamy
(P. A. Gowaty and D. W. Mock, Eds.).Ornithol.
1989. Intraspecificnestparasitismand extra-pair
copulationin LesserSnow Geese.Anim. Behav.
Monogr. No. 37.
37:74-89.
MOLLER,A. P. 1987. Copulation behaviour in the
LEBRET,
T. 1961. The pair formation in the annual
Goshawk,Accipitergentills.Anim. Behav.35:755763.
cycleof the Mallard (Anasplatyrhynchos
L.). Ardea
LACK,D. 1968. Ecologicaladaptationsfor breeding
49:97-158.
MosnY, H. S., AND C. O. HANDLEY. 1942. The Wild
LEFEBVRE,
E.A. 1977. LaysanAlbatrossbreedingbehavior.
LEWIS, R.A.
Auk 94:270-274.
1985.
Do Blue Grouse form leks? Auk
102:180-184.
LORENZ,
K. 1941. VergleichendeBewegungstudien
an Anatinen. J. Ornithol. 89:194-294.
MADDISON,
W. P. 1990. A model for testingthe correlated evolution of two binary characters:Are
gains or lossesconcentratedon certain branches
of a phylogenetictree?Evolution 44:539-557.
MADDISON,W. P., M. J. DONOGHUE,AND D. R. MAD-
DISON.1984. Outgroup analysisand parsimony.
Syst. Zool. 33:83-103.
MAHER,W.J. 1974. Ecologyof Pomarine, Parasitic
and Long-tailedjaegersin northern Alaska.Pacific Coast Avifauna, No. 37.
MAUNDER,J. E., AND W. THRELFALL.1972. The breed-
ing biology of the Black-legged Kittiwake in
Newfoundland.
Auk
89:789-816.
MCDONALD,
S. D. 1970. The breeding behaviorof
the Rock Ptarmigan.Living Bird 9:195-238.
MCINTYRE,
J.W. 1988. The CommonLoon. Spirit of
northern lakes. Univ. Minnesota Press, Minne-
apolis.
MCKINNEY,F. 1986. Mate guarding and the confidence of multiple paternity in waterfowl. Pages
411-419 in Acta XIX CongressusInter•ationalis
Ornithologici (H. Ouellet, Ed.). Ottawa, Ontario,
1986. National Museum of Natural Science, Ot-
Inland Fisheries, Richmond.
MUELLER,H.C. 1986. The evolution of reversed sex-
ual dimorphismin owls: An empirical analysis
of possibleselectivefactors.Wilson Bull. 98:387406.
NELSON,
J.B. 1966. The breedingbiologyof the Gannet, Sula bassana,on the BassRock, Scotland. Ibis
108:584-624.
NESBITT,
S.A. 1989. The significanceof mate lossin
Florida
Sandhill
Cranes.
Wilson
Bull.
101:648-
651.
NOBLE-ROLLIN,
D. 1975. Daily behaviourof the White
Stork. Dawn Song and All Day (World Bird ResearchStation, Glanton, Northumberland) 2:2328.
O'DONALD,
P. 1983. The Arctic Skua,a studyof the
ecologyand evolutionof a seabird.Cambridge
Univ. Press,Cambridge.
OHMART,R. D. 1973. Observationsof the breeding
adaptationsof the Roadrunner. Condor 75:140149.
ORING,L. 1982. Avian mating systems.Pages1-92
in Avian biology,vol. 6 (D. S. Farher,J. R. King,
and K. C. Parkes, Eds.). Academic Press, New
York.
PAGEL, M.D.,
AND P. H. HARVEY. 1988. Recent de-
velopmentsin the analysisof comparativedata.
tawa.
McKITRICK,
M.C. 1985. Pelvicmyologyof the kingbirds and their allies (Aves: Tyrannidae). Ann.
Carnegie Mus. 54:275-317.
MCKITRICK, M. C. 1990. Genetic evidence for mul-
tiple parentagein EasternKingbirds (Tyrannus
tyrannus).Behav. Ecol. Sociobiol. 26:149-155.
MCKITRICK,
M.C. 1991. Phylogeneticanalysisof avian hind limb musculature.
Misc. Publ. Mus. Zool.
The benefits
of communication
Q. Rev. Biol. 63:413-440.
PALMER,R. S. (Ed.). 1962. Handbook of North American birds, vol. 1. Yale Univ. Press, New Haven.
PALMER,R. S. (Ed.).
1988a. Handbook of North
American birds, vol. 4. Yale Univ. Press, New
Haven.
PALMER,R. S. (Ed.). 1988b. Handbook of North
American birds, vol. 5. Yale Univ. Press, New
Haven.
Univ. Mich., No. 179.
MCLENNAN, D. A., D. R. BROOKS,AND J. D. MCPHAIL.
1988.
Turkey in Virginia. Its habits and management.
EducationalDivision, Virginia Comm.Gameand
between
PAYNE,
R. B. 1969. Breedingseasons
and reproductive physiology of Tricolored Blackbirds and
840
MAgYC. McKrrRIC•<
Redwinged Blackbirds.Univ. Calif. Publ. Zool.
90:1-115.
differencesin varianceof breedingsuccess.
Am.
history and breeding behavior of the tinamou,
Nothoproctaornata.Auk 72:113-127.
PERDECK,
A.C. 1963. The early reproductivebehaviour of the Arctic Skua,Stercorarius
parasiticus
(L.).
51:1-15.
PITELKA,F. A., P.O.
TOMICH, AND G. W. TREICHEL.
1955. Breedingbehaviorof jaegersandowlsnear
Barrow, Alaska. Condor 57:3-18.
PLUMS,W. J. 1965. Observations on the breeding
biology of the Razorbill. Br. Birds 58:449-456.
POOLE,A. 1985. Courtship feeding and Osprey reproduction.Auk 102:479-492.
POOLEY,
A. C. 1977. Nest opening responseof the
Nile crocodileCrocodylus
niloticus.
J. Zool. (Lond.)
182:17-26.
PRATT,
H. 1970. Breedingbiologyof GreatBlueHerons and Common Egrets in central California.
Condor
lution
43:1781-1795.
SEALy,S. G. 1974. Breedingphenologyand clutch
size in the Marbled
114:447-452.
PEARSON,A. K., AND O. P. PEARSON. 1955. Natural
Ardea
SANDERSON,M. J., AND M. J. DONOGHUE. 1989. Pat-
terns of variation in levels of homoplasy.Evo-
PAYNE, R. B. 1979. Sexual selection and intersexual
Nat.
[Auk,Vol. 109
72:407-416.
Murrelet.
Auk 91:10-23.
SHERMAN,A. 1911. Nest life of the Screech Owl. Auk
28:155-168.
SHIELDS,
W. M. 1984. Barn Swallow mobbing: Self
defence,collateral kin defence,group defence,
or parental care?Anim. Behav.32:132-148.
SIEGFRIED,
W. R. 1976. Socialorganizationin Ruddy
and Maccoa
ducks. Auk
93:560-570.
SILVER,R., H. ANDREWS,AND G. F. BALL. 1985. Pa-
rental carein an ecologicalperspective:A quantitative analysisof avian subfamilies.Am. Zool.
25:823-840.
SPENCER,
O. R. 1943. Nesting habits of the Blackbilled
Cuckoo. Wilson
STEWART,
P.A.
Bull. 55:11-22.
1974. A nesting of BlackVultures.
Auk 91:595-600.
STONEHOUSE,
B.,ANDS.STONEHOUSE.
1963. The frigate bird Fregataaquilaof AscensionIsland. Ibis
103b:409-422.
STRAHL,
S.D. 1988. The socialorganizationand behaviour of the Hoatzin Opisthocomus
hoazinin
PRUM,R.O. 1990. Phylogeneticanalysisof the evolution of display behavior in the NeDtropical
central Venezuela.
Ibis 130:483-502.
manakins(Aves:Pipridae).Ethology84:202-231. STRAUCH,
J.G. 1978. The phylogenyof the CharadriQUINN,J. S. 1990. Sexual size dimorphism and paiformes(Aves):A new estimateusingthe method
rental care patterns in a monomorphicand diof charactercompatibility analysis.Trans. Zool.
morphic larid. Auk 107:260-274.
Soc. Lond. 34:263-345.
RAIKOW,R.J. 1978. Appendicular royologyand re- SUTHERLAND,C. A. 1963. Notes on the behavior of
lationshipsof the New World nine-primariedosCommon Nighthawks in Florida. Living Bird
cines(Aves:Passeriformes).Bull. Carnegie Mus.
2:31-39.
Nat. Hist. 7:1-43.
R•IKOW,R.J. 1982. Monophyly of the Passeriformes:
Test of a phylogenetichypothesis.Auk 99:431445.
SWOFFORD,
D.L. 1990. PAUP: Phylogeneticanalysis
using parsimony, version 3.0s. Illinois Natural
History Survey, Champaign.
THORESON,
A.C. 1964. Thebreedingbehaviorof the
RAIKOW,
R.J. 1987. Hindlimb myologyand evoluCassin Auklet. Condor 66:456-476.
tion of the Old World suboscinepasserinebirds
A.C. 1969. Observationson the breeding
(Acanthisittidae,Pittidae, Philepittidae, Eury- THORESON,
behaviourof the diving petrel Pelecanoides
u. urilaimidae). Ornithol. Monogr. No. 41.
natrix (Gmelin). Notornis 16:241-260.
REILLY,P. N., AND P. BALMFORD.1975. A breeding
study of the Little Penguin Eudyptulaminorin VANRHIIN,J.G. 1984. Phylogeneticalconstraintsin
the evolutionof parentalcarestrategiesin birds.
Australia.Pages161-187 in The biology of penNeth. J. Zool. 34:103-122.
guins(B.Stonehouse,
Ed.).UniversityParkPress,
VAN RHIIN, J.G. 1985. A scenario for the evolution
Baltimore.
RIDLEY,M. 1978. Paternal care. Anim. Behav. 26:904932.
RIDLEY,M. 1983. The explanation of organicdiversity.The comparativemethodandadaptationsfor
mating. ClarendonPress,Oxford.
RODGERS,
J. A., JR. 1980. Little Blue Heron breeding
behavior.
Auk 97:371-384.
RYAN,M. R., ANDJ.J.DINSMORE.1979. A quantitative
studyof thebehaviorof breedingAmericanCoots.
Auk 96:704-713.
SAGAR,P.M. 1979. Breeding of the Cape Pigeon
(Daptioncapense)
at the SnaresIslands. Notornis
26:23-26.
of socialorganizationin RuffsPhilomachus
pugnax
and othercharadriiformspecies.Ardea73.25-37.
VANRHIIN,J.G. 1990. Unidirectionality in the phy1ogenyof socialorganization,with specialreference
to birds.
Behaviour
115:153-174.
VEHRENCAMP,
S., B. S. BOWEN,AND R. R. KOFORD. 1986.
Breedingrolesand pairing patternswithin communal groupsof Groove-billedAnis. Anim. Behav. 34:347-366.
WALKINSHAW,
L.H.
1965. One hundred thirty-three
Michigan Sandhill Crane nests.Jack-PineWarbler 43:137-143.
WARHAM,J. 1975. The crestedpenguins.Pages189-
October
1992]
Phylogeny
ofAvianParental
Care
841
269 in The biology of penguins(B. Stonehouse, WittiNs, D. A., AND R. D. MORRIS. 1987. Parental
care of the Common Tern Sterna hirundo. Ibis 129:
Ed.). University Park Press,Baltimore.
WARnAM, J., B. R. KEELS, AND G. J. W•LSON. 1977.
Breedingof the Mottled Petrel. Auk 94:1-17.
WEIMERSKIRSCH,
H., P. JOUVENTIN,AND J. C. STAHL.
533-540.
W•LE•,R. H. 1974. Evolution of socialorganization
and life-history patternsamong grouse.Q. Rev.
Biol. 49:201-227.
1986. Comparativeecologyof the six albatross
E. J., AND T. J. CADE. 1964. Breeding
speciesbreedingon the Crozet Islands.Ibis 128: W•LLOVC•B¾,
behavior of the American Kestrel (Sparrow
195-213.
WELLER,M.W.
1958. Observations on the incubation
behavior of a CommonNighthawk. Auk 75:4859.
WERSCHKUL,
D.F. 1982a. Parental investment: Influ-
enceof nest-guardingby maleLittle BlueHerons
Promiscuous
behavior.
Condor
84:
WESTMORELAND,D., L. B. BEST,AND D. E. BLOCKSTEIN.
1986. Multiple-broodingasa reproductivestrategy: Time conservingadaptationsin Mourning
Auk
88:143-155.
103:196-203.
WIGGINS,D. A., AND R. D. MORRIS. 1986. Criteria for
female choice of mates:Courtship feeding and
paternal care in the Common Tern. Am. Nat. 128:
130:526-543.
W•NICL•R,D. W., AND J. R. WALTERS.1983. The determinationof clutchsizein precocialbirds.Curt.
Ornithol.
381-384.
Doves.
Condor
WINICLER,
D. W. 1987. A generalmodel for parental
care. Am. Nat.
Florida caerulea. Ibis 124:343-346.
WERSC•ICUL,
D. F. 1982b. Nesting ecologyof Little
Blue Heron:
Hawk). Living Bird 3:75-96.
WILSON,U. W., ANDD. A. MANVWAL.1986. Breeding
biologyof the RhinocerosAuklet in Washington.
1:33-68.
WITTENBERGER,
J. F. 1978. The evolution of mating
systemsin grouse.Condor 80:126-137.
WOLF,L. L., AND J. S. WOLF. 1971. Nesting of the
Purple-throated Carib Hummingbird. Ibis 113:
306-315.
WooDs,R.S. 1960. Notes on the nestingRoadrunner. Condor
62:483-484.
126-129.
APPENDIX
1. Charactersused in the analysis.
APPENDIX
1. M. iliotibialis mediaIls: (1) present;(0) absent.2.
M. iliotibialis lateralis,pars preacetabularis:(0) pres-
M. obturatoriuslateralis,parsdorsalis:(0) present;(1)
ent;(1) absent;(2) vestigial.3. M. iliotibialislateralis,
origin: (0) absent;(1) present.24. M. obturatoriusme-
pars acetabularis:(0) present;(1) absent;(2) aponeurotic; (A) 0 + 1.4. M. iliotibialis lateralis,pars postacetabularis: (0) present; (1) absent; (A) 0 + 1. 5. M.
diaIls, number of tendons of insertion: (0) one tendon;
iliotrochantericus caudalis: (1) reduced; (0) unre-
obturatorius medialis and obturatorius lateralis, distal
duced.6. M. iliotrochantericus
cranialis,stronglyfused
fusion: (0) yes; (1) no. 27. M. iliofemoralis internus:
(0) present;(1) absent.28. M. iliofemoralisinternus:
(0) "typical";(1) "unusuallyshortand broad."29. M.
arablens:(0) present;(1) absent.30. M. arablens,extent of origin: (0) limited to pectineal process;(1)
with M. iliotrochantericus caudalis: (1) fused; (0) un-
fused. 7. M. iliofemoralis externus:(0) present; (1)
absent. 8. M. femorotibialis externus, distal head: (0)
present;(1) absent.9. M. femorotibialisinternus, longitudinal division:(1) present;(0) absent.10. M. iliofibularis,ansa iliofibularis forms a single ligament:
(1) present;(0) absent.11. M. iliofibularis, ansailiofib-
ularisarmselongated:(1) present;(0) absent;(2) moderately elongate.12. M. flexor cruris lateralis,pars
1.
Continued.
absent. 23. M. obturatorius mediaIls, two heads of
(1) two tendons;(2) three tendons.25. M. obturatorius
mediaIls,enlargedin width: (0) no; (1) yes. 26. Min.
extendingfrom pectinealprocessto pubis;(2) one
origin from pectinealprocessand one from pubis.31.
M. arablens,
longitudinaldivision:(0) absent;(1) present. 32. M. gastrocnemius
parslateralis:(0) single;(1)
double;(A) 0 + 1.33. M. gastrocnemius
parsmediaIls,
accessoria:(0) present; (1) absent; (A) 0 + 1. 13. M.
flexor cruris lateralis,pars pelvica:(0) present;(1) absent. 14. M. flexor cruris lateralis,pars accessoria:
(1)
reduced; (0) not reduced; (?) absent. 15. M. caudofemoralis:(0) present;(1) absent;(2) poorly developed.
16. M. iliofemoralis:(0) present;(1) absent;(2) poorly
pateliar band: (0) present;(1) absent;(A) 0 + 1. 34.
developed;(A) 0 + 1. 17. M. flexor cruris mediaIls,
two distinctparts:(1) present;(0) absent.18. M. flexor
tibialis cranialis, number of tendons of insertion: (0)
bifurcated tendon; (1) one tendon. 38. M. extensor
cruris medialis and M. flexor cruris lateralis, tendons:
digitorumlongus,numberof headsof origin:(0) one
(0) fused; (1) unfused. 19. M. pubo-ischio-femoralis,
division into pars cranialisand pars caudalis:(1) divided; (0) not divided. 20. M. pubo-ischio-femoralis,
muscular slip: (0) absent; (1) present. 21. M. puboischio-femoralis, pars profundus divided into two
parts:(0) undivided; (1) divided; (2) intermediate. 22.
head (from tibia); (1) two heads(from tibia and fibula);
(2) two heads (from tibia and femur). 39. M. extensor
M. gastrocnemius
parsmediaIls,numberof heads:(0)
one head; (1) two heads;(A) 0 + 1. 35. M. gastrocnemius, fourth head: (0) absent; (1) present. 36. M.
gastrocnemius,
tendonof insertioncontributesto ossiftcationof the hypotarsus:(0) no; (1) yes. 37. M.
digitorum longus,hallucal tendon: (0) absent;(1)
present.40. M. fibularislongus:(0) present;(1) poorly
developed;(2) absent;(B) 0 + 2. 41. M. fibularis longus,tibial head:(0) present;(1) fibularheadonly;(2)
8•2
APPENDIX 1.
M_•¾ C. McKrrmcl<
Continued.
APPENDIX 1.
[Auk, Vol. 109
Continued.
brevis digiti IV: (0) present;(1) vestigial; (2) absent;
(C) 1 + 2. 66. M. lumbricalis: (0) absent; (1) present;
(2) weak or vestigial. 67. Feathers:(1) present; (0)
absent (to reflect monophyly of birds and thereby
(2) absent.44. M. flexor perforanset perforatusdigiti
III, vinculum: (0) present; (1) absent. 45. M. flexor excludeAncestor).68. Neognathmonophyly("dummy variable"):(1) reflectsmonophylyof the ingroup
perforanset perforatusdigiti II, relationshipto M.
(for actual synapomorphies,see Cracraft 1986, Craflexor perforanset perforatusdigiti III: (0) doesnot
craft and Mindell 1989);(0) all other taxa. 69. Paleogoverlapand concealFPPD3;(1) doesoverlap.46. M.
flexor perforanset perforatusdigiti II, numberof nath monophyly ("dummy variable"): (1) reflects
heads:(0) one head; (1) intermediate; (2) two; (3) three.
monophylyof the sistergroup of neognaths(for ac47. M. flexor perforanset perforatusdigiti II, origin
tual synapomorphiessee Cracraft 1986, Cracraftand
Mindell 1989);(0) all other taxa. 70. Mating system:
from ansailiofibularis: (0) absent;(1) present.48. M.
(0) monogamy;(1) polygyny;(2) polyandry;(3) promflexor perforatus digiti II, position: (0) deeply situiscuity; (A) 1 + 2; (B) 0 + 1; (C) 0 + 3. 71. Duration
ated; (1) superficial. 49. M. plantaris: (0) present; (1)
of pair bond: (0) seasonal;(1) brief; (2) longer than
absent; (A) 0 + 1. 50. M. plantaris: (0) "typical"; (1)
"brief" but less than one nesting effort; (3) longer
very powerfully developed.51.M. flexorhallucislonthan one season(ranging from acrosstwo seasonsto
gus,branchto hallux: (0) present;(1) lacking or weak.
life); (4) pair bond may be renewed annually but dis52. M. flexor hallucislongusand M. flexor digitorum
solvesbetweenseasons.
72. Mate guardingby males:
longus, type of flexor arrangement:see George and
(0) absent;(1) present.73. Resourcedefensepolygyny
Berger(1966:447)for descriptionof TypesI-VIII, and
(harem):(0) absent;(1) present;(A) 0 + 1.74. Lekking:
Betman (1984) for description of Type X (coded 9
herein); modificationfound in hummingbirdsis des- (0) absent;(1) present.75. Defenseof young/parental
care:(0) biparental; (I) uniparental (female); (2) unignated Type 0. 53. M. flexor hallucislongus,number
iparental (male); (3) double clutches;(4) no parental
of heads: (0) one head; (I) two heads; (2) three heads.
care; (A) 0 + 1. 76. Distinguishable reverse sexual
54. M. flexor digitorum longus,number of heads:(0)
dimorphism of any kind: (0) absent; (1) present. 77.
two heads; (1) three heads. 55. M. flexor digitorum
Males feed females during nest care: (0) no; (1) yes.
longus, size: (0) "typical"; (1) very powerful; (2) intermediate.56. M. flexor digitorum longus, location: 78. Incubation:(0) by female; (1) by both parents;(2)
by male only; (3) by neither parent. 79. Nest-building
(0) deeply situated;(1) superficially situated. 57. M.
popliteus:(0) present;(1) absent.58. M. flexorhallucis or nest-siteselection:(0) by female only; (1) by both
parents;(2) by male only. 80. Posthatching(prefledgbrevis:(0) present;(I) vestigial;(2) absent;(B) 0 + 2.
59. M. flexor hallucis brevis, number of tendons of
ing) care(feeding, as distinctfrom defense,character
insertion: (0) one; (1) two. 60. M. extensor hallucis
75): (0) female only; (1) both parents;(2) male only;
longus:(0) present;(1) absent.61. M. extensorhallucis (3) neither parent. 81. Postfledgingcare: (0) female
longus,number of heads:(0) two heads;(1) one head; only; (1) both parents;(2) male only; (3) neither. 82.
(A) 0 + 1.62. M. extensorhallucislongus,accessory: Group breeding: (0) absent;(1) present.83. Colonial
nesting:(0) absent;(1) present. 84. Posthatchingde(0) absent;(1) present. 63. M. abductor digiti II: (0)
velopment: (0) precocial;(I) altricial.
present;(1) absent;(2) vestigial.64. M. adductordigiti
II: (0) present; (1) weak; (2) absent. 65. M. extensor
arising from underlying musclesand from tibia. 42.
M. fibularislongus,branch to FPD3: (0) present;(1)
absent.43. M. fibularis brevis: (0) present;(1) weak;
October1992]
Phylogeny
ofAvianParental
Care
843
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October1992]
Phylogeny
ofAvianParental
Care
845
AI•I•ENOIX3. Character-changelists for behavioral
characters
(70-84) basedon Tree 1 (Fig. 2). The "ci"
refersto consistencyindex. Eachchangeis one step
in length. Arrows with double lines indicate transitionsthat arethe samefor all optimizations(ALL).
Arrows with single lines indicate transitionsthat
are not the samefor all optimizations(e.g. ACCTRAN). The "wt" refers to "within-terminal taxon."
See Methods for explanation of optimization routines.
Character 70 (ci = 0.667). ALL: node 102 0 •
3
Eulampis(a change from state 0 to state 3 between
node 102 and Eularnpis);
node 115 0 • 3 Dendragapus.
ACCTRAN: node 118 0 • 1 Ancestor; node 62 0 • 1
node 61; Rhea1 • 12 = A (wt); Crypturellus
1 • 12 =
A (wt); node 1140 • 1 Anas;Oxyura0 • 03 = C (wt);
Opisthocomus
0 • 01 = B (wt). DELTRAN: Rhea1 • 12
= A (wt); Crypturellus1 • 12 = A (wt); node 62 1 •
0 Nothoprocta;node 117 1 • 0 node 113; node 114 1
• 00xyura; Oxyura 0 • 03 = C (wt); Opisthocomus
1
• 01 = B (wt). MINF: Rhea1 • 12= A (wt); Crypturellus
1 • 12 = A (wt); node 62 1 • 0 Nothoprocta;
node 118
1 • 0 node 117;node 114 0 • 1 Anas;Oxyura0 • 03
= C (wt); Opisthocomus
0 • 01 = B (wt).
Character 71 (ci = 0.222). ALL: node 61 2 •
0 Rhea;
node 64 4 • 3 Pterodroma;
node 68 4 • 0 Podiceps;
node 69 4 • 3 Chen;node 74 4 • 3 Cepphus;
node 84
0 • 3 Grus;node 115 2 • 1 Dendragapus.
ACCTRAN:
0•0000
0•.•0•.
0•0000
node 117 2 • 0 node 113; node 83 0 • 4 node 78;
node 88 0 • 4 node 87; node 90 0 • 4 Ciconia; node
103 0 • 1 node 102; node 102 1 • 3 node 101; node
106 0 • 3 node 104; node 111 0 • 3 node 110; node
O0
109 3 • 4 Crotophaga;
node 112 0 • 1 Zenaida;Zenaida
1 • 12 = A (wt). DELTRAN: node 113 2 • 0 node 93;
000000
000000
000000
node 83 0 • 4 node 78; node 88 0 • 4 node 87; node
90 0 • 4 Ciconia; node 111 2 • 0 node 108; node 102
•.000•
0 • 3 node 101; node 102 0 • 1 Eularnpis;
node 104 0
000•00
4 Crotophaga;
Zenaida2 • 12 = A (wt). MINF: node
•0000
0000•
000000
000000
117 2 • 0 node 113; node 83 0 • 4 node 78; node 88
0 • 4 node 87; node 90 0 • 4 Ciconia; node 102 0 •
• 3 Picoides;
node 1092 • 3 Geococcyx;
node 109 2 •
3 node 101; node 102 0 • 1 Eularnpis;
node 104 0 • 3
Picoides;
node 109 0 • 3 Geococcyx;
node 109 0 • 4
Crotophaga;
node 112 0 • 1 Zenaida;Zenaida1 • 12 =
A (wt).
Character 72 (ci = 0.143). ALL: node 102 1 • 0
Eularnpis;node 106 1 • 0 node 104; node 114 0 • 1
Anas. ACCTRAN: node 62 0 • 1 node 61; node 85 0
oo
oo
oo
• 1 node 84; node 80 1 • 0 Rissa; node 113 0 • 1
node 112. DELTRAN and MINF: node 61 0 • 1 Rhea;
.ooEE
node83 0 • 1 node 78;node 79 0 • 1 Rynchops;
node
112 0 •
oo
gooo
•
0•.0000
•
000000
•
•000•.•
•00•0
0•00
000000
000000
1 node
Character 74 (uninformative).
Character 75 (ci = 0.600). ALL: node 118 0 • 2 node
62; node 102 0 • 1 Eularnpis.
ACCTRAN: node 117 0
• 1 node 116; node 114 1 • 00xyura; Opisthocomus
1 • 12 = A (wt). DELTRAN and MINF: node 114 0 •
1 Anas;node 116 0 • 1 node 115; Opisthocomus
1•
000000
000000
111.
61.
0000•
•0•00
1 node
Character 73 (ci = 1.000).ALL: node 62 0 •
000000
00•00
'•
•
•
12 = A (wt).
Character 76 (ci = 0.500). ALL: node 82 0 •
corarius 1; node 101 0 •
1 Ster-
1 node 99.
Character 77 (ci = 0.250). ALL: node 81 0 •
1 node
846
MARYC. MCKITRICK
APPENDIX 3.
Continued.
APPENDIX 4.
[Auk,Vol. 109
Continued.
80. ACCTRAN: node 93 0 • 1 node 92; node 108 0 •
(Thoreson 1969). 16. Pygoscelis
adeliae(Ainley and
Schlater1972,Derkson 1977,Ainley et al. 1983).17.
Eudyptes,
all spp. (Warham 1975). 18. Eudyptulaminor
101; node 105 0 • 1 Corvus.
(Reilly and Balmford1975).19.Spheniscus
magellanicus
Character 78 (ci = 0.375). ALL: node 69 1 ==•0 Chen; (Boswalland MacIver 1975).20. Gaviaimmer(Mcintyre
node 97 1 ==•0 Accipiter;node 105 1 ==•0 Tyrannus. 1988).21.Podiceps
nigricollis
(R.W. Storer,pers.comm.).
ACCTRAN: node 118 0 • 3 Ancestor; node 118 0 •
22. Fregataaquila(Stonehouseand Stonehouse1963).
2 node 62; node 117 0 • 1 node 113; node 103 1 • 0
23. Phalacrocorax
auritus(Palmer 1962).24. Anhingaannode 102; node 101 0 • 1 node 99. DELTRAN: node
hinga(Burger et al. 1978). 25. Sula bassanus
(Nelson
1 node 107; node 102 1 • 0 Eulampis.DELTRAN and
MINF: node 89 0 • 1 Leptoptilus;
node 1020 • 1 node
118 3 • 2 node 62; node 117 3 •
1 node 113; node
100 1 • 00tus; node 102 1 • 0 Eulampis;node 117 3
• 0 node 116. MINF: node 118 1 • 3 Ancestor; node
118 1 • 2 node 62; node 100 1 • 00tus; node 102 1
1966). 26. Ardea herodias(Pratt 1970, Mock 1979). 27.
Butoridesstriatus(Palmer 1962). 28. Florida caerulea
(Rodgers1980,Werschku11982a,
b). 29.Mycteriaamericana(Palmer 1962, Kah11972). 30. Ciconiaciconia(Haverschmidt 1949, Noble-Rollin 1975). 31. Leptoptilus
• 0 Eulampis;node 117 1 • 0 node 116.
Character 79 (ci = 0.286). ALL: node 117 0 • 1 node
crumeniferus
(Kahl 1966).32. Plegadis
autumnolis
(Bayminor(Brown
113;node 89 1 • 2 Mycteria;node 96 1 ==•0 Chordeiles; nard 1913, Palmer 1962). 33. Phoeniconaius
and Root 1971). 34. Cathartesaura (Coles 1944, Palmer
node 102 1 • 0 Eulampis.
ACCTRAN:node 118 0 • 2
node 62; node 71 1 • 2 node 66; node 106 1 • 0 node
105. DELTRAN: node 62 0 • 2 node 61; node 65 1 •
20ceanodroma;node 105 1 • 0 Tyrannus.MINF: node
62 0 • 2 node 61; node 66 1 • 2 node 65; node 105
1 • 0 Tyrannus.
Character 80 (ci = 0.750). ALL: node 102 1 • 0
Eulampis.
ACCTRAN: node 118 0 • 3 Ancestor;node
118 0 • 2 node 62; node 117 0 • 1 node 113. DELTRAN: node 118 3 • 2 node 62; node 117 3 • 1 node
113; node 117 3 • 0 node 116. MINF: node 118 1 •
3 Ancestor; node 118 1 • 2 node 62; node 117 1 • 0
node
116.
Character 81 (ci = 0.333). ALL: node 118 1 • 2 node
62; node 83 1 ==•3 node 78; node 70 3 ==• 1 node 69;
node 74 3 • 2 node 73; node 94 1 ==• 3 Florida; node
96 1 • 2 Chordeiles;node 103 1 • 3 Chaetura; node
112 1 ==•2 Zenaida; node 117 1 ==•0 node 116.
Character 82 (ci = 0.250). ALL: node 103 0 •
1
Chaetura; node 105 0 ==• 1 Corvus; node 109 0 ==• 1
Crotophaga;
node 115 ==•Opisthocomus.
Character 83 (ci = 0.200). ALL: node 85 0 ==•1 node
84; node 69 1 • 0 node 68; node 93 0 • I node 92;
1988a).35. Coragyps
atratus(Stewart 1974).36. Gymnogyps
californicus
(Palmer 1988a).37. Accipitergentilis
(Moller 1987,Palmer1988a).38. Buteo
jamaicensis
(Fitch
et al. 1946, Palmer 1988b). 39. Pandionhaliaetus(Green
1976,Poole 1985,Birkhead and Lessells1988).40. Falco
sparverius
(Willoughby and Cade 1964,Palmer 1988b).
41. Chencaerulescens
(Finney and Cooke 1978,Cooke
et al. 1981, Lank et al. 1989). 42. Anasplatyrhynchos
(Lebret 1961, Goodburn 1984, McKinney 1986). 43.
Oxyurajamaicensis
(Siegfried 1976,Joyner 1977). 44.
Dendragapus
obscurus
(Wiley 1974,Wittenberger1978,
Lewis 1985).45. Lagopus
mutus(McDonald 1970).46.
Canachites
canadensis
(Ellison 1973).47. Bonasaumbellus
(Gladfelterand McBurney1971,Wittenberger1978).
48.Meleagris
gallopavo
(MosbyandHandley1942,Dalke
et al. 1946). 49. Opisthocomus
hoazin(Strahl 1988).50.
Gruscanadensis
(Walkinshaw 1965, Nesbitt 1989). 51.
Fulicaamericana
(Ryan and Dinsmore 1979).52. Rynchops
niger(Burger1981,Quinn 1990).53. Stercorarius
pomarinus
(Pitelkaet al. 1955,Maher 1974).54. Stercorarius
parasiticus
(Perdeck1963,O'Donald1983).55.
Larusmarinus(Butler and Janes-Butler1983). 56. Rissa
1 Crotophaga. tridactyla
(Hodges1969,MaunderandThrelfall 1972).
Character 84 (ci = 0.250). ALL: node 117 0 ==•1 node
57. Sternahirundo(Wiggins and Morris 1986, 1987).
node 95 0 •
1 node 94; node 109 0 •
113; node 88 1 • 0 node 85; node 91 1 •
conaius;node 96 1 • 0 Chordeiles.
APPENDIX 4.
References
0 Phoeni-
used for each taxon.
58. Alca torda(Plumb 1965,Harris and Birkhead 1985).
59. Uria aalge(Johnson1941,Birkheadet al. 1985,
Hatchwell 1988).60.Cepphus
columba
(Drent 1965).61.
Brachyramphus
marmoratum
(Sealy 1974). 62. Ptychoramphus
aleuticus
(Thoreson1964).63.Cerorhinca
monocerata(Wilson and Manuwal 1986).64. Fraterculaarctica
(Ashcroft 1979).65. Zenaidamacroura(Westmoreland
etal. 1986).66.Coccyzus
erythropthalmus
(Spencer,1943).
1. Ancestor,Crocodylus
(Hunt 1975, Pooley 1977). 2.
californianus
(Woods1960,Ohmart 1973,
Rheaamericana
(Bruning 1974).3. Crypturellus
boucardi 67. Geococcyx
Folse and Arnold 1978). 68. Crotophagasulcirostris
(Lancaster1964). 4. Nothoprocta
ornata(Pearsonand
Pearson 1955). 5. Diomedeaimmutabilis(Fisher 1971,
(Vehrencampet al. 1986).69. Otusasio(Sherman1911,
Allen 1924).70. Bubovirginianus
(Errington 1932,Keith
Lefebvre 1977).6. Phoebetria
fusca(Weimerskirschet
al. 1986).7. Daptioncapense
(Sagar1979).8. Fulmarus 1977). 71. Chordeilesminor (Bent 1940, Weller 1958,
Dexter 1961, Sutherland 1963). 72. Chaeturapelagica
glacialis
(Hatch 1987,1990).9.Procellaria
parkinsoni
(Imjugularis
(Wolf
ber 1987). 10. Puffinuspuffinus(Palmer 1962, Harris (Dexter1952,Fischer1958).73.Eulampis
and Wolf 1971).74. Colapres
auratus(Burns1900).75.
1966, Lack 1968). 11. Pterodromainexpectata(Warham
et al. 1977). 12. Oceanitesoceanites
(Palmer 1962). 13.
Picoides
villosus(Kilham 1966, 1968, 1969).76. Tyrannus
Fregettatropica(Beckand Brown 1971).14. Oceanod- tyrannus(McKitrick 1990, pers. observ.).77. Corvus
romaleucorrhoa
(Palmer 1962). 15. Pelecanoides
urinatrix brachyrhynchos
(Good 1952).