Phylogenetic Patterns of Parental Care in Calidridine Sandpipers
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The Auk 116(4):1107-1117, 1999 PHYLOGENETIC PATTERNS OF PARENTAL CARE IN CALIDRIDINE SANDPIPERS OKSANA A. BOROWIK • AND DEBORAH A. MCLENNAN 2'3 •RoyalOntario Museum, 100 QueenõPark, Toronto,Ontario M5S 2C6, Canada;and 2Departmentof Zoology,Centre For Comparative Biology and Biodiversity, University of Toronto,25 HarbordStreet, Toronto,Ontario M5S 3G5, Canada ABSTRACT.--Weexamined the sequenceof parental-careevolution in calidridinesandpip- ersby mappingparental-care characters onto the two treesproduced by a maximum-like- lihood and parsimonyanalysis of moleculardata. Our analysisindicated that asymmetric biparentalcare (male incubates and caresfor young,female incubates) is plesiomorphicfor the group.This state has been maintained in at least10 of the 22 speciesinvestigated. There havebeen four changesfrom the ancestralcondition: (1) three to four increasesin female carecoupled with a completeloss of male care;(2) an increasein femalecare with the main- tenanceof male care,producing symmetric biparental care; (3) an increasein femalecare followed at a later date by three independentlosses of male care in Calidrismelanotos, C. fuscicollis,and Tryngitessubruficollis; and (4) a decreasein female care in C. pusilla.Received 23 May 1997, accepted20 April 1999. QUESTIONSABOUT the evolutionof avianpa- systemsin all birds (vanRhijn 1990:160),(2)fe- rental care have fascinated researchers for de- male-only care is extremelyunlikely to evolve cades,in part becausebirds show such a wide into anothercare pattern,and (3) biparental range of strategiesand becausethe factors careis unlikely to evolveinto either type of uni- shapingthe evolutionof thesestrategies are parentalcare if both parentsshare incubation very complex(Clutton-Brock 1991, Ligon 1993, duties.Both models make very explicitpredic- Ketterson and Nolan 1994, Temrin and Sill•n- tionsabout the sequenceof parental-careevo- Tullberg1994). Given this complexity,one way lution that canbe examinedwithin a compar- to disentangleall of the potentialfactors is to ative framework. break the systeminto simple,definable com- The phylogeneticcomparative approach is a ponentsand model the interactionsamong powerfulway to disentanglecharacter origin them.There are two generalscenarios for the from subsequentcharacter modification and to sequenceof parental-careevolution in Aves. study the sequenceof charactermodification The first (Fig. 1A) proposesthat uniparental over long periodsof time (Ridley 1983,Wann- care alwaysarises from biparentalcare, with torp 1983, Brooks 1985, Brooks and McLennan the sexof the singleparent being determined 1991).One of the strengthsof this approachis by the relativecosts and benefits of careversus that it allows the collection of data about the desertionto eachparent (Jenni1974, Pitelka et types of evolutionarytransitions that hap- al. 1974,Emlen and Oring 1977).Hild•n (1975) pened most often, that happened once and postulatedthat the intermediatestate between were maintained for long periods of time, and biparentaland uniparental care might be a sys- thatnever happened within a givenclade. This tem in which the female rapidly laid two informationmay then be used to examinethe clutchesof eggs(double clutching), each clutch beingcared for by oneparent. Van Rhijn (1985, predictions of evolutionary models and to 1990;see also Handford and Mares 1985) pro- highlightareas in the modelsthat need to be poseda more complicatedscenario (Fig. lB). In modified (Brooks and McLennan 1991, 1994; its simplestform, this scenariomakes three McLennan 1996). general predictions:(1) male parental care is McKitrick(1992) investigated the macroevo- the precursorto the radiationof parental-care lutionary patterns of parental-careorigin and diversificationacross major avian lineages. She concludedthat the ancestralparental-care sys- 3Address correspondence to this author.E-maih tem for Aves was either asymmetricor sym- [email protected] metricbiparental care (biparentalor femalein- 1107 1108 BOROWIKAND MCLENNAN [Auk, Vol. 116 (A) Imale parental care]-'•'---•- biparental care• femaleparentalcare a I biparentalcareI increasedcarebysecond maleparental care filr•parent i [femaleparentalcare ] FIG.1. Pathwaysof parental-careevolution postulated by (A) Emlenand Oring (1977)and (B) van Rhijn (1990).Bold arrows denote the mostprobable transitions, and light arrowsdenote unlikely transitions. cubation + biparental care of young). In no althoughwe can infer its presencebecause casedid the analysissupport the hypothesis maledesertion of the clutchpresumably could that male-onlycare was the ancestralstate for not existprior to theorigin of increasedfemale birds. Sz6kelyand Reynolds(1995) narrowed investment.In the secondcase, biparental care the scopeof the investigationto oneavian lin- is detectableon a macroevolutionaryscale (still eage,the Charadriides(excluding Labroidea). present in extant species).The comparative The macroevolutionarypatterns indicated that phylogeneticanalysis thus indicated that mod- biparental care (not male-only) was plesio- els of parental-careevolution should incorpo- morphicfor this groupof shorebirds,reinforc- rate informationabout the factorsinfluencing ing McKitrick'sconclusion that paternal care the rate of a population'smovement through couldnot be viewedas the precursorto all oth- thebiparental state into the explanatoryframe- er parental-caresystems. Within the group, the work. dominant transitionswere male-only to bipa- McKitrick (1992) examined patterns of pa- rental (5 to 11 times),male-only to female-only rental care on a large scale,whereas Sz6kely (6 to 8 times)and biparentalto male-only(2 to and Reynolds(1995) narrowed their focusto 6 times).Transitions from biparentalto female- the shorebirds.Continuing in this vein,we in- only careand vice versawere very rare (0 to 3 vestigatedthe sequenceof parental-careevo- timeseach). The data confirmedprevious sug- lutionwithin onegroup of shorebirds,the cal- gestionsof a link between male-only and bi- idridine sandpipers.We chosethis group be- parentalcare and confirmedvan Rhijn's(1990) causerelationships within it have been ana- predictionthat biparentalto female-onlycare lyzed phylogenetically(Borowik 1996), and should be rare. becausesandpipers display a wide rangeof pa- Theanalysis also highlighted two interesting rental-care strategies. We were interested pointsfor furtherresearch. First, there has been mainly in (1) discoveringwhether the domi- a trend toward increasingfemale carerelative nantsequences of parental-careevolution with- to malecare in shorebirds.The authors hypoth- in the sandpiperswere similarto thosedetect- esized that sexual selection favors male deser- ed on a largerphylogenetic scale, and (2) using tion becauseextrapair copulations present the the powerof the comparativephylogenetic ap- only meansopen to a male to enhancehis re- proachto highlightareas for futureresearch. productive success.Second, the transition "male-only to female-only" care is far more MATERIALS AND METHODS likely to occurthan is the sequence"male-only to biparentalto female-only"care (seeFig. 1). Data on parentalcare were obtainedfrom Pitelka The only differencebetween these two transi- et al. (1974),Johnsgard (1981), Sz6kely and Reynolds tionsis the persistenceof the intermediatebi- (1995),and sourceslisted in the Appendix.As sug- parentalstage. In the first case,biparental care gested by Temrin and Sil16n-Tullberg(1994), we is transitoryfrom a phylogeneticperspective, mapped parental-carebehavior separately for the October1999] ParentalCare in Sandpipers 1109 (ancestor2) J Femaleonly incubates [] I FI•. 2. Parental-carestates optimized onto the most-parsimonioustree for calidridinesandpipers based on a maximum-likelihoodanalysis of 1,645characters (1,045 base pairs from cytochromeb, 600 basepairs from ATPase6; Borowik1996). Outgroups = BlackTurnstone (Arenaria melanocephala) and Ruddy Turnstone (A. interpres).Female care: white box = femaleincubates, black box = femaleincubates and caresfor young; malecare: white box = maleincubates and cares for young,black box = no malecare. Crosses = lossof male parentalcare, asterisk = reductionin femalecare, and F = increasein femalecare. See Figure 5 for the four equallyparsimonious optimizations of parental-careevolution in the Philornachuspugnax + Lirnicolafalcinellus + C. acurninata clade. sexesso that we couldstudy the interactionbetween of the genusCalidris and alsoin the additionof C. differentlevels of maleand femalecare. Based upon rninuta,C. ptilocnernis,C. subrninuta,C. tenuirostris, the data collected,we divided parentalcare into two Limicolafalcinellus, Aphriza virgata, and Philomachus characters:(1) male care(either male care absentor pugnaxto the analysis.Arenaria melanocephala and male incubatesand caresfor young),and (2) female Arenariainterpres were used as outgroups.Optimi- care (either female incubatesor female incubatesand zationswere checkedon McClade 3.01, using the caresfor young).Parental-care states were coded dif- Acctranand Deltran algorithms,but more options ferentlyfrom thoselisted in Sz•kelyand Reynolds werediscovered in a hands-onanalysis because com- (1995)for the followingspecies: (1) femaleincuba- puterprograms did not allow a combinationof both tion was added to Calidrisalpina, C. canutus,C. rnar- Acctranand Deltran optimizations for onecharacter. itima, C. pusilla,and C. ruficollis;and female incuba- tion and care for young was added to C. bairdii,C. RESULTS mauri,and C. minutilla(see Appendix). The evolutionof parental-carebehaviors