Recognizing and testing homology of courtship displays in storks (Aves: Ciconiiformes ciconiidae).
The utility of behavioral traits as phylogenetic characters depends on an accurate assessment of homology and translating behavioral observations into a matrix of characters for cladistic analysis. Translation involves identifying behavioral units to define as characters, assigning relative weights to the characters, and ordering character-state changes. The activities of assessing homology and coding data as characters are interdependent: an initial hypothesis of homology is needed to define characters, and a cladistic analysis of the coded characters tests the hypothesis of homology. The test is via the congruence of a given character with the remaining characters in the data matrix (Patterson 1988) or relative to a tree based on a different dataset (Maddison and Maddison 1992). In this paper, I explore the issue of assessing and testing the homology of presumably innate behaviors and the practical problems associated with defining characters from behavioral observations, focusing on social display behaviors in storks (Aves: Ciconiiformes: Ciconiidae). The basic question is how to transform observations of social display behaviors in different species of birds into characters that are useful in inferring relationships among species and tracing the evolution of displays in the study group.
In this study, I use a tree based on DNA-DNA hybridization distances as an independent estimate of phylogeny. Because DNA-DNA hybridization produces obligate distance data, many systematists, particularly cladists, deny the utility of the method as a means of estimating phylogenetic relationships (e.g., DeSalle and Brower 1997). However, the effectiveness of DNA-DNA hybridization can be defended on both theoretical and empirical grounds. The theoretical defense rests on the fact that DNA-DNA hybridization distances can be analyzed nonphenetically, if the following criteria are satisfied: (1) an outgroup is included in the data matrix, and all ingroup taxa are reciprocally compared to the outgroup; and (2) the algorithm chosen for analysis does not assume a uniform evolutionary rate across lineages (e.g., the FITCH algorithm in PHYLIP). Under these conditions, the resulting tree groups taxa according to apomorphic, not plesiomorphic, similarity (Sheldon 1994). Empirically, carefully constructed trees based on DNA-DNA hybridization data are virtually always highly congruent with phylogenies inferred from character data (Powell 1991; Krajewski and Fetzner 1994; Lanyon and Hall 1994; Slikas 1997). In regard to molecular character data, the strengths and weaknesses of mitochondrial sequence data and DNA-DNA hybridization distances are complementary: mitochondrial sequence characters typically yield strongly-supported resolution of relationships between closely related species, while DNA-DNA hybridization distances yield better resolution of more distant relationships (e.g., between avian genera; Slikas 1997).
The avian family Ciconiidae, or storks, includes 19 species distributed in tropical and subtropical regions around the world. The family is distinctive, characterized by several shared morphological and behavioral features, including long legs, a stout bill, 12 primary feathers, 12 tail feathers, and common social behaviors (Hancock et al. 1992). Recent phylogenetic analyses based on cytochrome b sequences and DNA-DNA hybridization distances strongly support the monophyly of the group (Slikas 1997). The available data on display behaviors in storks are unusually extensive and detailed. Over an 1 l-year period, M. P. Kahl collected behavioral data for all stork species, mostly from field observations (Kahl 1966, 197la,b, 1972a-e, 1973). He focused especially on social displays during courtship and nesting. Kahl explicitly hypothesized homology of behaviors across species, assigning the same name to displays in different species that he considered to be derived from a common behavior in their nearest ancestor. Kahl used his behavioral data, supplemented by a consideration of superficial morphological features, to revise the classification within the stork family, reducing the number of recognized genera from 11 to six ([ILLUSTRATION FOR FIGURE 1 OMITTED]; Kahl 1971a, 1972d).
Wood (1984) coded Kahl's behavioral descriptions as discrete binary and multistate characters and analyzed the resulting data matrix phenetically. Wood's phenetic tree supports the genera defined by Kahl, but conflicts with Kahl's classification in the inferred relationships among genera. Relationships among stork species also have been estimated based on cytochrome b sequences and DNA-DNA hybridization data (Slikas 1997). Although the optimal trees based on the two molecular datasets are not identical, conflicting nodes are weakly supported in one or both trees. The best-fit DNA-DNA hybridization tree is identical in topology to Wood's phenogram based on behavioral data [ILLUSTRATION FOR FIGURE 2 OMITTED].
All 19 extant stork species employ a species-specific repertoire of display behaviors, many associated with courtship and nesting (Kahl 1971a). Displays are more numerous, more frequently performed, and often more highly ritualized in species that nest in dense colonies, including Ciconia abdimii and species in the genera Anastomus, Mycteria, and Leptoptilos (although in Leptoptilos species, pairs sometimes nest singly). In these predominantly colonial species, a male-female pair bond is established each breeding season, presumably with a different mate. Other storks, including Ephippiorhynchus senegalis, E. asiaticus, and Jabiru mycteria, nest as single pairs. Pairs remain together in the nonbreeding season, and pair bonds are apparently maintained over several breeding seasons. These solitary-nesting birds are much less demonstrative at the nest (Kahl 1973; Hancock et al. 1992).
In most stork species, males establish themselves on a potential nest site at the start of the breeding season; in Anastomus, Mycteria, and Leptoptilos species the unmated males perform advertising display(s): Display Preening (Mycteria spp. only), Advertising Sway (Anastomus spp. only), and Swaying Twig-Grasping (all Mycteria, Anastomus, Leptoptilos spp.). In Display Preening, the advertising male rhythmically performs the motions of preening the wing feathers, alternating between wings, although his bill often does not touch the feathers. In the Advertising Sway, the male stands on the nest site, bends forward until his bill is pointed almost between his feet, then stiffly shifts his weight back and forth, lifting each foot slightly with each sway. In the similar Swaying Twig-Grasping display, the bird stands on the nest site, bends forward until the bill almost touches the substrate, then sways rhythmically from side to side, usually grasping lightly at twigs at the end of each sway (Kahl 1971a, 1972a,b,e).
In the next phase of courtship, a lone female approaches an unmated male. A male on a nest site will react in a hostile manner to the approach of any bird, male or female (Kahl 1971a). In species of Mycteria, Anastomus, and Leptoptilos, the approaching female usually performs a display, presumably to appease the male. In Mycteria species, the female performs a Gaping display, walking toward the male or standing with her bill open. In Mycteria and Leptoptilos species, the female approaches the male in a Balancing Posture, with the body horizontal, neck partially extended, bill pointed down, and wings spread (Kahl 1966, 1972a,b). The male typically rebuffs the approaching female, but she returns repeatedly, and is eventually accepted on the nest site (Kahl 1971a).
Both the male and female participate in nest building in all stork species. In Ciconia species, during pair formation and for a few days thereafter, the male gives a Head-Shaking Crouch display to an approaching female, crouching on the nest site and vigorously shaking his head from side to side. This display is most ritualized and elaborate in Ciconia abdimii, the only Ciconia species to nest in dense colonies (Kahl 1971a, 1972c-d). In the Ephippiorhynchus species and Jabiru mycteria, because the male and female usually remain together outside the breeding season, the pair establish a nest site simultaneously. Kahl (1973) observed no pair-formation displays in these species.
In all storks, care of young is performed by both male and female. Throughout the breeding season, a mutual, species-specific, Up-Down display is performed, usually when one of the pair returns to the nest after an absence (Kahl 1971a; Hancock et al. 1992). The Up-Down display is one of the few displays common to most (possibly all) stork species. The display varies considerably among species, but typically involves movement of the head and neck up and down or horizontally, accompanied by bill clattering and/or vocalizations. The Up-Down is most highly ritualized in Ciconia ciconia: the performing bird clatters its bill loudly and rapidly, while throwing its head up and back, until its bill is pointing toward its tail, then forward again to the normal position (Kahl 1971a, 1972c,d). The Up-Down is performed relatively infrequently in Ephippiorhynchus species and J. rnycteria, presumably because pairs remain together year-round, so the pair bond does not need to be reinforced as frequently (Kahl 1971a, 1972d). In fact, the Up-Down was not observed at all in Ephippiorhynchus senegalis, although Kahl (1973) argues that the display is probably performed by this species, but was not observed due to inadequate observations at the correct time of year. The Ephippiorhynchus species and J. mycteria share a unique display among storks, the Flap-Dash, which is performed away from the nest, usually while the pair forages. One member of the pair dashes wildly around, flapping its wings vigorously, usually ending facing its mate and standing there for several seconds with its wings widely spread (Kahl 1971a, 1973). All stork species have a ritualized copulation display, Copulation Clattering, which varies in several details across species.
In addition to the displays described above, which are performed between mates, storks also perform social displays directed toward other conspecifics or even individuals of a different species (Kahl 197 la). The Forward Threat and Forward-Clattering Threat, for example, are performed between unmated adults, usually of the same sex, and are presumably aggressive. The Anxiety Stretch is a display common to all species, performed by a bird on the nest in response to the approach of an unfamiliar object, such as a vehicle. The display involves stretching the neck forward and peering down at the approaching object; details of the display vary among species (Kahl 1971a, 1972d).
The social displays performed by storks are stereotypical, that is, the performance of the display is virtually identical each time it is executed. One caveat is that some displays are performed at different "levels of intensity," so some elements in the display might be dropped or subdued on some occasions, presumably when the stimulus is insufficient to invoke the full display (Tinbergen 1952; Kahl 1966). Although Kahl did not explicitly survey the variability of displays among conspecifics, he did not note any variation among individuals within the populations that he studied (Kahl 1966, 1971b, 1972a-e, 1973). He mentioned one possible example of variation between populations: Kahl observed an Up-Down display given by a Ciconia nigra individual in a resident South African population in which the individual clattered its bill, while C. nigra breeding in Europe do not bill-clatter during the Up-Down (Kahl 1972d). In general, ritualized avian displays are thought to be species specific and uniform within species (Tinbergen 1952).
MATERIALS AND METHODS
The social display behaviors described by Kahl (1966, 1972a-c,e, 1973) were coded as binary or multistate characters (Tables 1,2). Each display was coded as a binary character with the states (1) present and (0) absent. In addition, complex displays were broken into component elements and each element treated as a separate character. All multistate characters were coded as unordered. Two analyses were performed: one in which all characters were assigned a weight of unity, and one in which multistate characters were weighted inversely to the number of states (i.e., a multistate character with n states was assigned weight 1/[n - 1]; Swofford 1993). A branch-and-bound parsimony analysis of the behavioral data matrix was performed using PAUP (Swofford 1993), with the character ordering and weighting described above. Trees are unrooted. No outgroup was included, because comparable behavioral data are not available for potential outgroup species.
The behavioral characters also were mapped parsimoniously onto a best-fit tree of relationships based on a matrix of DNA-DNA hybridization distances ([ILLUSTRATION FOR FIGURE 2 OMITTED]; Slikas 1997). With this approach, the congruence of each behavioral character with the DNA-DNA hybridization tree was measured. Mapping was done using MacClade (Maddison and Maddison 1992). The DNA-DNA hybridization tree was selected for character-mapping, because resolution of relationships at the base of the stork clade is more strongly supported in this tree than in the most-parsimonious or maximum-likelihood trees based on cytochrome b sequences (Slikas 1997). The DNADNA hybridization tree is rooted with two outgroup taxa: Cathartes aura (Turkey Vulture), representing the family Cathartidae, the New World vultures, and Plegadis falcinellus (Glossy Ibis), representing the family Threskiornithidae, the ibises and spoonbills. The relationship of storks to other avian families is highly debated, and both the New World vultures and ibises/spoonbills have been advocated as the sister group to storks, based on different sets of evidence (Ligon 1967; Olson 1979; Sibley and Ahlquist 1990; Griffiths 1994; Seibold and Helbig 1995). In any case, the same tree topology was obtained with either or both outgroups included in the DNA-DNA hybridization data matrix (Slikas 1997).
Phylogeny based on Behavioral Characters
The maximum-parsimony analysis of the behavioral data matrix with all characters assigned unit weight yielded 48 most-parsimonious trees with a consistency index (CI) of 0.81; the analysis with multistate characters weighted by 1/(n - 1) yielded 24 most-parsimonious trees (CI = 0.80), all identical to trees obtained in the equally weighted analysis. The expected CI for a tree with this number of terminal taxa is 0.59 (Sanderson and Donoghue 1989). In both analyses, the most-parsimonious trees differed from each other in the following: (1) the branching sequence among J. mycteria, E. senegalis, and E. asiaticus; (2) the branching sequence among Mycteria species; and (3) relationships among the three clades Mycteria, Leptoptilos, and Anastomus. In addition, maximum-parsimony trees resulting from the analysis with all characters given unit weight differed with respect to relationships among the three Leptoptilos species. The ambiguity in the relationships among Jabiru and the Ephippiorhynchus species is due in part to missing data; 14 of the 46 characters were scored as unknown for E. senegalis, because neither copulation nor the Up-Down display was observed for this species (Kahl 1973).
In the 24 most-parsimonious trees based on the analysis with multistate characters downweighted [ILLUSTRATION FOR FIGURE 3 OMITTED], the genera defined by Kahl based on his behavioral observations ([ILLUSTRATION FOR FIGURE 1 OMITTED]; Kahl 1971a, 1972d) are supported as monophyletic groups. The 24 most-parsimonious trees show conflicting resolution of relationships among genera, except for the pairing of Jabiru and Ephippiorhynchus, and the pairing of the Jabiru-Ephippiorhynchus clade with the Ciconia clade. The latter pairing is strongly supported in the best-fit tree based on [TABULAR DATA FOR TABLE 2 OMITTED] DNA-DNA hybridization distances and the maximum-likelihood and maximum-parsimony trees based on cytochrome b sequences (Slikas 1997), but the pairing is inconsistent with Kahl's definition of stork tribes (Kahl 1971a, 1972d). Kahl grouped the "giant" storks (Leptoptilos, Jabiru, and Ephippiorhynchus) together in the tribe Leptoptilini, based on morphological similarities, and he placed the Ciconia species in a separate tribe, the Ciconiini.
Wood (1984) coded Kahl's behavioral data as a character matrix and performed a phenetic analysis of the coded data. Wood's tree is largely congruent with the most-parsimonious trees from this study, except in relationships among species within the genus Ciconia. I performed a parsimony analysis of Wood's (1984) behavioral data matrix, which yielded five most-parsimonious trees, all congruent with most-parsimonious trees from both the weighted and unweighted analyses in this study.
The trees obtained from analysis of the behavioral data matrix are unrooted, because no outgroup is included and the characters are unordered. Because an unrooted tree is congruent with several different rooted trees, the behavior-based trees cannot give a definite resolution of basal relationships in the stork family. However, the unrooted trees obtained in this study are all congruent with the basal resolution of relationships in the best-fit DNA-DNA hybridization tree [ILLUSTRATION FOR FIGURE 2 OMITTED], in which the family is split into two clades, Anastomus-Leptoptilos-Mycteria and Jabiru-Ephippiorhynchus-Ciconia. The unrooted behavior-based trees are incongruent with the alternative resolutions of basal relationships in the most-parsimonious and maximum-likelihood trees based on the cytochrome b sequence data (Slikas 1997).
In my coding of Kahl's behavioral data, the split of the family into the two clades, Anastomus-Leptoptilos-Mycteria and Jabiru-Ephippiorhynchus-Ciconia, is supported by changes in two characters: presence/absence of the Swaying Twig-Grasping and Snap displays (characters 9 and 14, respectively; Table 1). These two displays are common and unique to Anastomus, Leptoptilos, and Mycteria species. A Jabiru-Ephippiorhynchus-Ciconia clade is supported only by the absence of traits. The pairing of Jabiru and Ephippiorhynchus is supported by three characters in the behavioral data matrix: the characteristic Flap-Dash display (character 19), one component of the Copulation Clattering display (character 36), and one component of the Up-Down display (character 44). The Ciconia species are united by four characters, including the characteristic Head-Shaking Crouch (character 46) and elements of the Copulation Clattering display (characters 32, 34, 35).
The pairing of the genera Leptoptilos and Mycteria is found in one-half of the most-parsimonious trees obtained from analysis of the behavioral data matrix, and this pairing is supported by two characters: presence of the Balancing Posture (character 1) and drooping of the undertail coverts in the Snap Display (character 16). The alternative Mycteria and Anastomus pairing proposed by Kahl (1971a, 1972d) appears in the remaining half of the most-parsimonious trees and is supported by three characters: one component of the Swaying Twig Grasping display (character 13), one component of Copulation Clattering (character 30) and one component of the Up-Down display (character 42). Kahl (1971a) emphasized particularly the similarity of the Copulation Clattering and Up-Down displays between Mycteria and Anastomus species in justifying his tribe Mycteriini, comprising these two genera. The DNA-DNA hybridization data support a Mycteria + Anastomus pairing, with relatively high bootstrap support (88%), but no sequence data were obtained for either Anastomus species ([ILLUSTRATION FOR FIGURE 2 OMITTED]; Slikas 1997). Given the strength of the bootstrap support in the DNA-DNA hybridization tree and considering the ambiguity of the behavioral data, the resolution ((Mycteria, Anastomus), Leptoptilos) is most strongly supported by the available data. This resolution implies some homoplasy in the behavioral characters as coded for this study. For example, the Balancing Posture display was either lost in Anastomus species or gained independently in Leptoptilos and Mycteria.
Mapping Behavioral Characters onto the DNA-DNA Hybridization Tree
To analyze patterns of evolutionary change in the behavioral characters, all were parsimoniously mapped onto the best-fit tree based on DNA-DNA hybridization distances [ILLUSTRATION FOR FIGURE 2 OMITTED]. The congruence of each character with this tree can be measured by its CI. Of the 46 characters in the behavioral data matrix, 13 have a consistency index less than one when mapped onto the DNA-DNA hybridization tree (Table 1). In terms of percentage of homoplastic characters, the amount of homoplasy in the behavioral characters is typical for phylogenetic datasets (Sanderson and Donoghue 1989; de Queiroz and Wimberger 1993).
Stork display behaviors exhibit substantially different levels of variability across species; within species, any given display is essentially invariant, based on Kahl's extensive observations (Kahl 1966, 197la,b, 1972a-e, 1973). Although difficult to quantify, the amount of interspecific variation and amount of homoplasy in display behaviors suggest a common pattern. The most variable/homoplastic behaviors either are not associated with courtship or reproduction (Anxiety Stretch) or occur late in the temporal sequence of courtship and nesting (Up-Down, Copulation Clattering). The displays that are uniform across species and consistent with phylogeny are those that occur earlier, either while the male is advertising (Display Preening, Advertising Sway) or while the female is seeking acceptance at the nest (Balancing Posture, Gaping, Flying Around, Head-Shaking Crouch). The average CI per character for early courtship displays (Balancing Posture, Gaping, Flying Around, Advertising Sway, Swaying Twig-Grasping, Snap Display, Display Preening, and Head-shaking Crouch) is 0.91, while the average CI for all other displays is 0.69. These averages were calculated excluding characters that are either invariant or autapomorphic for terminal taxa (Table 1; characters 3, 8, 11, 21, 22, 28, 29, 37, 43). A [[Chi].sup.2] test (2 x 2) of the association between CI (CI [less than] 1, CI = 1) and display type (early courtship, other) yielded a probability of about 15%, indicating that the proposed association of high CI with early courtship displays is not strongly supported. The high P-value probably results because most characters in the data matrix, regardless of type, have a perfect CI.
An association between high CI and early courtship displays is interesting, because such an association could be driven by selection. Early courtship displays are vital in the recognition of conspecifics, so selection might prevent loss of the trait and maintain its uniformity within a species. Interestingly, five of the six displays included in the early courtship category (all except Head-shaking Crouch) are performed exclusively by species in the genera Mycteria, Leptoptilos, or Anastomus. These nine species all nest colonially, and individuals select a mate at the beginning of each breeding season. The remaining eight species, except Ciconia abdimii, typically nest as single pairs and possibly maintain pair bonds over several breeding seasons (Hancock et al. 1992). Presumably, selection for a mechanism for recognizing conspecifics would be stronger in the colonial nesting than in the solitary-nesting species.
Homology of Display Behaviors
Avian displays are believed to be innate, based principally on their remarkable stereotypy. In storks, nestlings give greeting and begging displays similar to displays in adults, even when reared in isolation, supporting the hypothesis that at least some displays in storks are primarily or completely innate (Kahl 1966). Although learned behaviors can be useful in reconstructing phylogenetic relationships, particularly at the species level (Payne 1986; Papaj 1993), innate behaviors generally are more conservative and thus potentially useful in inferring relationships at higher taxonomic levels. Recent studies testing the homology of courtship display behaviors in manakins (Prum 1990), pelicaniformes (Kennedy et al. 1996), and ducks (Foster et al. 1996) demonstrated that the displays in these groups were no more homoplasious than morphological characters.
In this study, phylogenetic analysis of a data matrix of behavioral characters coded from Kahl's descriptions of stork display behaviors yielded trees that are mostly congruent with phylogenies based on two independent datasets, DNA-DNA hybridization distances and cytochrome b sequences. Further, the nodes in the most-parsimonious behavior-based trees that conflict with the DNA-DNA hybridization and/or cytochrome b-based trees are weakly supported by the behavioral data. The congruence of trees based on the coded behavioral data with those based on independent datasets provides additional evidence for the usefulness of display behaviors as phylogenetic characters.
Homology assessment for behavioral traits generally follows criteria analogous to those applied to morphological traits. In particular, Remane's (1952) criteria for recognizing homologous traits can be applied to behaviors as well as to morphological features. Remane's three criteria are (1) position with respect to a landmark; (2) special quality; and (3) connection by evolutionary intermediates. For behavioral traits, "position" was interpreted by Tinbergen (1959) as the temporal position of a component behavior in a ritualized sequence, such as "tail wagging" in the greeting ceremony of gulls. By this criterion, if in different species the "tail wagging" component occurs at the same position in a behavioral sequence, relative to other components in the sequence, it can be hypothesized to be homologous in these species (Wenzel 1992). The criterion of "special quality" applies to the complexity and stereotypy of a behavior, that is, a hypothesis of homology based on similarity is stronger for more complex and ritualized behaviors than for simple or highly variable ones. The third criterion refers particularly to ritualized behaviors. Recognizing the more "primitive" homologs of highly derived, ritualized behaviors is aided by the existence on intermediates. In his assessments of homology, Kahl implicitly applies Remane's second and third criterion by limiting his analysis to stereotypical, complex behaviors and using the range of variation in a display to facilitate homology assessments among highly derived display behaviors. In coding Kahl's behavioral descriptions as discrete characters, I invoked Remane's first criterion of "position" to homologize components within displays.
Ritualized behaviors such as the courtship/nesting displays of storks are hypothesized to be derived from certain frequently performed, innate behaviors, used in activities such as feeding, fighting, or nest-building (Tinbergen 1952). Given this origin, ritualized behaviors might be considered to be particularly susceptible to convergence, because the simple behaviors from which they are derived are often quite similar across even distantly related species. For example, fighting behaviors are often ritualized, and in birds usually involve stretching the neck, pointing the bill toward the opponent, and snapping or clattering the bill. Thus, a ritualized aggressive display might appear quite similar in different bird species without necessarily being homologous. The problem is comparable to distinguishing paralogous from orthologous genes in comparing a member of a gene family across species, or recognizing convergence arising from historical and functional constraints in a morphological feature. Some courtships displays performed by storks are similar to displays in other avian families. For example, herons (family Ardeidae) perform a Snap Display very similar to the Bill Snap of storks (Hancock et al. 1992). Ibises and spoonbills (Threskiornithidae) perform several displays closely similar in form and function to displays in storks: Display Preening, Bill Popping (= Bill Snap in storks), Greeting (= Up-Down), Bowing display (= Balancing Posture), and Nest-Covering display (= Nest-Covering display; Hancock et al. 1992). The Shoebill (Balaenicipitidae) gives a bill-clattering display similar to the Up-Down display of storks (Kahl 1972d), and the Secretarybird (Sagittariidae) performs an Up-down Bowing display similar to the Up-Down of storks and a Wings-Open display similar to the Flap-Dash (Kemp 1995). The similarity of these display behaviors might reflect homology, but since the phylogenetic relationships among these groups of birds are currently unresolved, it is difficult to assess the likelihood of homology versus convergence. The chance of a mistaken assessment of homology probably increases as comparisons are made between more distantly related taxa, because the opportunities for convergent evolution multiply. Analyses of ritualized display behaviors within two avian families (Pipridae, Prum 1990; Ciconiidae, this study) and across families within an order (Pelicaniiformes, Kennedy et al. 1996) suggest that convergence is uncommon in avian displays at these taxonomic levels.
Behavioral and Morphological Evolution
In general, ritualized display behaviors are believed to function in communication among conspecifics, to express intentions, and to coordinate reproductive activity in mated pairs (Tinbergen 1952; Van Tets 1965; Kahl 1971a). Some display behaviors feature the flaunting of a conspicuous morphological trait, presumably to enhance the impact and specificity of the signal (Tinbergen 1952). Assuming this hypothesis, morphological traits featured in displays are expected to be under selection to bolster the effectiveness of the display, that is, behavior can drive morphological change. Support for this hypothesis was found by Prum (1990) in his study of lek display behaviors in manakins, a family of Neotropical suboscine passerine birds in which all behaviorally known species are polygynous, and the males display on leks. Some manakin species have distinctive plumage characters that are utilized in the lek display, including lengthened tail feathers or white wing patches. Prum (1990) mapped both the displays and associated plumage traits onto a phylogeny based on a parsimony analysis of syringeal characters. He discovered several independent cases in which displays evolved prior to the plumage traits featured in the display, a pattern consistent with the hypothesis that the plumage traits evolved under selection for their role in the display.
Among storks, the data regarding this hypothesis are more ambiguous. In the Flap-Dash display performed by Jabiru and Ephippiorhynchus species, the wings are spread, prominently displaying the white flight feathers. The effect is most dramatic in the Ephippiorhynchus species in which the rest of the wing feathers are black. Jabiru and Ephippiorhynchus are the only stork species to have white flight feathers (Hancock et al. 1992), but because both the display and the plumage trait is confined to these three species, the sequence of evolution cannot be determined. In E. asiaticus and J. mycteria, the wings are also spread in the Up-Down display; the Up-Down was not observed in E. senegalis. Among the other storks, only Ciconia abdimii and C. episcopus spread their wings in the Up-Down. Thus, for the character of "spread wings" in the Up-Down display, two reconstructions are equally parsimonious: (1) "spread wings" arose in the common ancestor to the combined Ephippiorhynchus-Jabiru-Ciconia clade and was subsequently lost on the branch leading to the Ciconia ciconia-maguari-nigra clade (assuming nigra pairs with ciconia and maguari); or (2) "spread wings" arose twice, independently in the ancestor to Jabiru/Ephippiorhynchus and Ciconia abdimii/episcopus. In the first reconstruction, the display arose before the associated plumage trait of "white flight feathers," supporting the hypothesis that the evolution of the plumage trait was driven by its display function; the alternative reconstruction neither supports nor contradicts the hypothesis.
Few other morphological traits in storks are specifically highlighted in displays. The Leptoptilos species and J. mycteria possess an inflatable throat sac that is often inflated when an individual is "excited," but this trait is not featured in any particular display. Thus, analysis of stork displays appears to provide no unambiguous evidence addressing the hypothesis that selection for enhanced signaling effectiveness can drive the evolution of morphological traits.
Issues of Character Coding
The coding of behaviors as discrete characters is not straightforward (McKitrick 1994). To accommodate the observed variation across species in some behavioral traits requires the use of multistate characters. A multistate character can be coded alternatively as a number of dependent binary characters; a character with n states translates to n - 1 binary characters. With either coding, to equalize the contributions of a multistate character and an independent binary character to the total tree length, an n-state character (or each of the n - 1 binary characters) must be assigned a weight inversely proportional to n - 1. Differential weighting is necessary, because an n-state character must undergo a minimum of n - 1 steps on a tree. This weighting scheme assumes that every independent character, binary or multistate, should contribute equally to total tree length, an arguable premise.
Ordering of character states is another difficult issue. For most multistate characters in this data matrix, the states correspond to different frequency or intensity levels in performance of the trait. Ordering of these states would impose the assumption that the behavior evolves along a gradient of frequency or intensity, that is, that a low-frequency/intensity state is always intermediate between an absent state and a high-frequency/intensity state. Because discontinuous evolutionary change in frequency or intensity of a behavior seems plausible, I did not order these character states.
In the absence of explicit ordering of character-state transformations, direction of character evolution can be assessed only by rooting the tree. Unfortunately, the behavioral data matrix does not include an outgroup, because the necessary data for plausible outgroup species are lacking. A particularly interesting question in the evolution of stork behavior is whether solitary or colonial nesting, and the presumably associated wealth of courtship display behaviors, is symplesiomorphic. The well-supported basal bifurcation in the storks splits the family into two equally sized clades with contrasting nesting habits: the Mycteria-Leptoptilos-Anastomus group includes only highly colonial species that share a number of characteristic courtship displays, and the Ephippiorhynchus-Jabiru-Ciconia group includes species with a variety of nesting habits, ranging from highly colonial (C. abdimii) to solitary, with most species at the latter end of the spectrum. Resolving the direction of evolution in nesting behavior requires identifying the sister group to storks, an open and highly debated issue. Candidate sister groups include the ibises and spoonbills (Threskiornithidae), a widespread group of colonially nesting, wading birds; the Shoebill (Balaeniceps rex), an African species with solitary habits; and the New World vultures (Cathartidae), scavengers that nest as single pairs. Given the diverse and contrasting characteristics of these potential sister groups, each would give a different reconstruction of the evolution of nesting and feeding behavior in stork species. A better resolution of relationships within and among avian orders is needed to address questions in life-history evolution in these birds.
For the storks, the available data on display behaviors are unusually complete and consistent. Over an 11-year period, Kahl made observations of all species, mostly in field settings. He described the displays in a consistent fashion and homologized displays across species. Few behavioral datasets are as extensive and detailed, but the data matrix is still incomplete, and population-level variation in behaviors was not assessed. These shortcomings underscore a basic problem in using behavioral data as phylogenetic characters - for a given set of taxa, a complete behavioral data matrix is generally much more time consuming to collect than a morphological or molecular dataset. Behavioral datasets can be compiled from the work of several researchers, but under such circumstances, assessing homology of behaviors and coding the data can be difficult unless the behaviors are described consistently, in sufficient detail, and with explicit comparison to potentially homologous behaviors in closely related species.
TABLE 1. List of 46 behavioral characters. Coded characters are based on descriptions of display behaviors by Kahl (1966, 1971a, 1972a-e, 1973). Names are identical to those assigned by Kahl. All displays were coded as present or absent. In addition, component elements of complex behaviors were coded as separate characters; these are indicated below by the initials of the display name, followed by a description of the component element. Characters that have a CI [less than] 1 when mapped parsimoniously onto the best-fit DNADNA hybridization tree [ILLUSTRATION FOR FIGURE 3 OMITTED] are preceded by an asterisk and followed by the value of the CI.
*1. Balancing Posture (BP): (0) absent; (1) present. CI = 0.5
2. BP, bill pointed vertically down: (0) no; (1) yes.
3. BP, legs bent, body lowered, bill lifted in "scooping" motion: (0) no; (1) yes.
*4. BP, vocalizations: (0) absent; (1) present. CI = 0.5
5. BP, bill snaps/rattles at beginning of display: (0) no; (1) sometimes; (2) usually.
6. Gaping: (0) absent; (1) present for brief period after [female] enters nest; (2) present for extended period.
7. Flying Around: (0) absent; (1) infrequent; (2) common.
8. Advertising Sway: (0) absent; (1) present.
9. Swaying Twig-grasping (STG): (0) absent; (1) present.
10. STG, tips of wings slightly raised: (0) no; (1) sometimes; (2) usually.
11. STG, dorsal neck balloon exposed: (0) no; (1) yes.
12. STG, neck, head swayed left-to-right: (0) no; (1) sometime; (2) usually.
13. STG, performed together by [female] and [male]: (0) no; (1) yes.
14. Snap Display (SD): (0) absent; (1) present.
15. SD, head shaken: (0) no; (1) yes.
*16. SD, undertail coverts drooped: (0) no; (1) yes. CI = 0.5
17. Display Preening (DP): (0) absent; (1) present.
18. DP, bill snapped: (0) no; (1) uncommon; (2) common.
19. Flap-Dash: (0) absent; (1) present.
*20. Erect Gape (EG): (0) absent; (1) present. CI = 0.5
21. EG, vocalizations: (0) no; (1) yes.
22. Anxiety Stretch (AS): (0) absent; (1) present.
*23. AS, vocalizations: (0) absent; (1) present. CI = 0.5
*24. AS, wings spread: (0) no; (1) partially; (2) fully. CI = 0.65
25. AS, orients 90 [degrees] to disturbing object: (0) no; (1) yes.
26. AS, undertail coverts displayed: (0) no; (1) sometimes; (2) usually.
*27. AS, bill snapped: (0) no; (1) yes. CI = 0.5
28. AS, neck puffed, tongue bone lowered: (0) no; (1) yes.
29. Copulation Clattering (CC): (0) absent; (1) present.
30. CC, [male] knocks bill against [female]'s: (0) no; (1) softly; (2) roughly.
*31. CC, [female]'s wings open: (0) to wrist; (1) fully. CI = 0.5
32. CC, [male] shakes head: (0) no; (1) weakly; (2) strongly.
33. CC, [male] clatters bill: (0) no; (1) yes.
34. CC, [male] clatters bill in neck ruff of [female]: (0) no; (1) yes.
35. CC, [male] clatters bill: (0) loudly; (1) softly.
36. CC, [male] clatters bill: (0) rapidly; (1) slowly.
37. Up-Down (UD): (0) absent; (1) present.
*38. UD; wings spread: (0) no; (1) partially; (2) fully. CI = 0.5
*39. UD, head, neck swayed side to side: (0) no; (1) yes. CI = 0.3
*40. UD, head, bill: (0) thrown upward, then lowered. (1) pointed down, then raised; (2) pointed down; (3) held in normal position. CI = 0.75
*41. UD, bill clattered: (0) in normal position; (1) as head raised; (2) as head lowered. CI = 0.65
42. UD, bill gaped: (0) no; (1) yes.
43. UD, body horizontal throughout display: (0) no, (1) yes.
44. UD, undertail coverts fanned: (0) no; (1) yes.
*45. UD, vocalizations: (0) none; (1) whistles; (2) hissing; (3) squeaks, mooing; (4) honking. CI = 0.8
46. Head-shaking Crouch: (0) absent; (1) present.
This work is based on my dissertation research at the University of Pennsylvania, Department of Biology. I thank my advisors E H. Sheldon and F. B. Gill for intellectual and financial support, as well as for their comments on the manuscript. The manuscript was improved further by comments from M. P. Kahl, M. McKitrick, L. Whittingham, and two anonymous reviewers. The work was funded in part by grants from the Frank M. Chapman Memorial Fund (American Museum of Natural History), American Ornithologists' Union Research Awards Program, and National Science Foundation grants BSR 9020183 and 9207991 to F. H. Sheldon and F. B. Gill.
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