Using behavioural characters in phylogeny reconstruction

Ethology Ecology & Evolution 14: 129-139, 2002

Using behavioural characters in phylogeny reconstruction

A.E. STUART

1,4,

F.F. HUNTER

2

and D.C. CURRIE

3

1

Department of Zoology, University of Toronto, Canada Department of Biological Sciences, Brock University, St. Catharines, Canada 3 CBCB, Royal Ontario Museum, Toronto, Canada 2

Behaviour remains underrepresented in phylogeny reconstruction, possibly because the term ‘behaviour’ incorporates a wide range of phenomena, not all of which are equally applicable to understanding evolutionary history. We assessed the character homology (i.e., potential problems with coding) and homoplasy (i.e., lability or convergence) for each of four types of behaviour (behavioural categories, reaction stimuli traits, the specific movements of animals and quantitative information relating to each of these behaviour types) and determined the broad applicability of each behavioural type for phylogeny reconstruction. When using behaviour to reconstruct a phylogeny we recommend the following order of behavioural types: (1) animal movements; (2) quantitative components (providing that the animal movements are homologous); (3) reaction stimuli traits; (4) behavioural categories.

KEY WORDS:

behaviour, phylogenetics, homology, homoplasy, evolution.

Introduction . . . . Behavioural types . . Behavioural categories Reaction stimuli . . Animal movements . Quantitative information Implications . . . . Acknowledgments . . References . . . .

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INTRODUCTION

The application of phylogenetics has increased markedly in the past decade; however, the use of behavioural data in phylogeny reconstruction remains underrepresented. During the 1970’s and 1980’s, questions were raised about whether 4 Send correspondence to: A.E. Stuart, Department of Ecology and Evolutionary Biology, Haworth Hall, 1200 Sunnyside Ave., Lawrence, KS 66045. Ph: (785) 864-5788, Fax: (785) 864-5321 (E-mail: [email protected]).

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behavioural data could or should be used to address macroevolutionary questions. Some argued that behavioural homology is more difficult to establish because behaviours were said to either be more labile (ATZ 1970, ARONSON 1981, BARONI URBANI 1989) or more subject to convergence than other types of data (ATZ 1970, ARONSON 1981, CARPENTER 1987, BARONI URBANI 1989). However, phylogenies reconstructed with behavioural data have been highly congruent with phylogenies based on morphological or molecular data (e.g., MCLENNAN et al. 1988, PRUM 1990, MCLENNAN 1993, PATERSON et al. 1995, KENNEDY et al. 1996, STUART & HUNTER 1998, MCLENNAN & MATTERN 2001). Further, recent studies assessing the validity of using behaviour in phylogenetic study have shown no reason to assume a priori that behaviour is any more subject to convergence than other types of data (WENZEL 1992, DEQUEIROZ & WIMBERGER 1993, WIMBERGER & DEQUEIROZ 1996, MCLENNAN & MATTERN 2001). Despite these studies, there remains an ‘ingrained cultural avoidance of behavior by many systematists’ (BUCHHOLZ & CLEMMONS 1997). The term ‘behaviour’ represents a wide range of phenomena, predominantly because animal behaviours are assessed in different ways depending on the question under investigation. It is this broadness of the term ‘behaviour’ that may contribute to the under-representation of behaviour in phylogeny reconstruction. In this paper, we divide the term ‘behaviour’ into four separate types: behavioural categories (PROCTOR 1996), reaction stimuli traits (MAYR 1976), the specific movements of an animal (MAYR 1976) and quantitative information of these behavioural types. Characters from each of these four behavioural types are heritable and variable and therefore can theoretically be used to reconstruct a phylogeny. However, it seems probable that different types of behavioural data are not equally useful for understanding evolutionary history. The goal of this paper is to assess the potential of each of these four behavioural types in phylogeny reconstruction. In this paper, we define each behavioural type, discuss character homology (i.e., potential problems with coding each behavioural type into phylogenetic characters) and homoplasy (i.e., lability or convergence) and examine the broad applicability of each behavioural type for phylogeny reconstruction. Homologous behaviours are those that arise from a common ancestor through descent (WENZEL 1992), which can ultimately only be determined a posteriori from a phylogenetic analysis (BROOKS & MCLENNAN 1991, WENZEL 1992, LAUDER 1994). Practically, phylogenetic characters and character states are chosen based on some a priori assumptions of homology (see WENZEL 1992 for discussion), and these assumptions are tested by the resultant phylogeny. There are at least two possible reasons that a character state is homoplasious: the a priori assumption of homology is incorrect or the character state is convergent. This paper is predominantly aimed at behaviourists or macroevolutionary biologists interested in constructing a phylogeny that uses any behavioural characters. However, we hope other fields of behavioural biology will benefit from the discussion of different behavioural types.

BEHAVIOURAL TYPES

Behavioural categories Behavioural categories are general terms that describe suites of behaviours that share some broad phenomena, usually, but not always, relating to function

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(PROCTOR 1996). The specific details of these broad terms are not necessarily the same among taxa. For example, the phrase “lekking behaviour” is a broad term that groups all taxa in which males hold a territory without any resources for the females. The term does not distinguish among the behaviours performed by individuals of a given species that serve to maintain a lek. The phylogenetic character “lekking behaviour” with states, (0) present; (1) absent, would group all animals that lek, regardless of the way the lek is established, maintained or the behaviours that occur while on the lek. This character will be convergent among many taxa. Cannibalism is also a behavioural category describing taxa whose individuals eat members of their own species. The character, “cannibalism” with states, (0) present; (1) absent, does not distinguish between adult male lions eating young after taking over a harem, female spiders that eat males after mating, or species whose individuals cannibalize weak or sick individuals or the manner in which individuals prey upon, capture or eat their prey. Other similar examples include: aggressive behaviour, monogamous vs. polygamous behaviour, cooperative breeding and gregarious behaviour. Behavioural categories are rarely thought to be homologous in a phylogenetic sense (WENZEL 1992, PROCTOR 1996). The terms represent phenomena that are likely to be distributed among a wide range of taxa, and thus their selection is, in effect, intended to maximize the probability of homoplasy (PROCTOR 1996), not to denote shared derived character states. Thus, we believe that broad behavioural terms should not be used as characters for phylogeny reconstruction.

Reaction stimuli One obvious component of behaviour is the ability of animals to react selectively to specific stimuli (‘perceptual traits’ of MAYR 1976). The objects that promote a reaction are often easy to characterize. MAYR (1976) uses the example of predatory wasps whose prey objects are spiders, caterpillars or sawfly larvae. These objects will induce a predatory response in some species of wasps, but not in others. By determining which species of prey is used by different wasp species, this information can be coded as a phylogenetic character. Another example is the type of building material used by animals to build a structure. If an individual selects and manipulates a particular type of material appropriate for building a structure, discriminating against other types of materials, then the type of building material can be coded as a character. This component of behaviour is thus a description of the object(s) that elicit a given behavioural reaction (e.g. species of prey, type of building material). When coding characters for phylogeny reconstruction, there is no reason to assume a lack of homology in traits that elicit a response. Thus, the character ‘Type of building material: (0) organic, (1) mineral’ would potentially be homologous. However, these traits may be prone to homoplasy (MAYR 1976). MAYR suggests that an evolutionary switch from one type of prey to another may not be exceedingly difficult. TABER’s (1994) data supports this hypothesis; he studied the life history and host utilization traits in 11 species of plant lice (Rhopalosiphum) and found that of 12 behavioural characters studied, none of the possibly conserved traits were those involving choice of the host plant taxa. Similarly, CARPENTER (1987) indicated that the character ‘paper type’ is not particularly informative when constructing a phylogeny of the wasps, because the character varies within genera of

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the Vespinae. The paper in a wasp nest is either pliable or brittle depending on whether the wood fibres (the objects that elicit nest building) collected are sound or rotten. Although homology is ultimately determined a posteriori from a phylogeny reconstructed with many characters (LAUDER 1994), it is worthwhile considering the potential homoplasy of reaction stimuli traits before reconstructing a phylogeny.

Animal movements Another obvious type of behaviour is the specific movement of an individual and its body parts during the course of any given behaviour (‘locomotory components’ of MAYR 1976). Behavioural repertoires, such as mating, feeding, or building behaviour are an aggregation of numerous smaller behavioural units. Evolution can potentially act on each behavioural unit over time, eventually culminating in the present-day behavioural repertoire of an animal. Thus, analyzing behavioural repertoires tells an ‘evolutionary story’ that can be deciphered by searching for shared derived character states. WENZEL (1992) states “if the complex movements of several species take the same distinct form in the same context and appear to be largely innate, they may be thought of as homologous”. DEQUEIROZ & WIMBERGER (1993) performed a thorough comparison of the levels of homoplasy of behavioural and morphological data. They compared the mean consistency index (CI) of behavioural characters and morphological characters and found that behaviour is no more homoplastic than morphology. Because they were looking at the mean CI of individual characters, there was no constraint on the number of characters included in their analyses. As such, some analyses used had very few behavioural characters. Additionally, DEQUEIROZ & WIMBERGER (1993) intentionally chose a broad definition of behaviour, which included all four categories described here. To assess animal movement data specifically, we searched for papers where animal movement data was used to construct entire phylogenies and the outcome compared to phylogenies constructed with other data (i.e., morphological and/or molecular). Nine such studies were found representing a variety of species and behaviours (Table 1). In all these studies, characters are delimited based on details of the specific movements of animals during their respective behaviours and all of these studies find behavioural data to be highly congruent with other types of data (see references in Table 1). For example, PRUM (1990) used 29 characters relating to the detailed description of lek display behaviour in 21 species of Neotropical Manakins. When the behavioural characters were analyzed alone, and when combined with syringeal characters (morphological traits), the results were highly congruent with the independent syringeal hypothesis of phylogeny. SLIKAS (1998) was the only study to find behaviour less reliable than other data. However, in her study, only behaviours late in the sequence of stork courtship behaviours had higher levels of homoplasy than DNA-DNA hybridization data; behaviours occurring early were congruent with phylogenetic relationships and showed little homoplasy. The congruency of animal movement phylogenies with phylogenies based on other data indicates that animal movement data are reliable indicators of evolutionary history. Further, because there is no significant difference (paired t-test: t = 0.54, P > 0.05) between the consistency indices (CI) of the respective datasets (Table 1), animal movements are also no more subject to homoplasy than other types of data.

Behaviour in phylogeny construction

133 Table 1.

A list of reconstructed behavioural phylogenies including authors, taxa, behaviours studied, number of characters in each analysis, and other data used for comparison and consistency indices (CIs). Consistency indices for the comparison data were either found in the original paper or in cited references within as noted. EBERHARD (1982) was not used for the statistical test. When data was not available for other references, a CI of 1.00 was used (†). All authors found the topology of the behavioural phylogenies to be congruent with that of the other data used. Reference

EBERHARD (1982)

Study organism

Behaviour

Spiders

MCLENNAN et Gasterosteid al. (1988) and fishes MCLENNAN (1993) ARNTZEN & Newts SPARREBOOM (1989)

# of

Data of

characters

comparison

CI

CI

Web-building

10

Adult morphology

N/A

N/A

Reproductive

27

Biochemical, morphological

0.90*

0.67*

Courtship

16

Biochemical

0.81

N/A†

behaviour other data

PRUM (1990)

Neotropical manakins

Display

29

Morphological

0.78!

0.90‡

PATERSON et al. (1995)

Albatrosses, petrels, penguins

Behaviour, life history

72

Molecular

0.52

0.53

KENNEDY et al. Pelecaniforms (1996)

Social behaviour

37

Morphological, molecular

0.74

0.67§

SLIKAS (1998)

Storks

Courtship displays

42

DNA-DNA hybridization

0.85

N/A†

STUART & HUNTER (1998)

Black flies

Cocoon spinning

14

Cytological, morphological

0.92

1.00

* MCLENNAN (2000) personal communication. ! 15 uninformative characters removed from PRUM (1990), which reduced the behavioural CI from 0.85 to 0.78. ‡ PRUM unpubl. data in DEQUIEROZ and WIMBERGER (1993). § CRACRAFT (1985), SIEGEL-CAUSEY (1988).

No references were found that refute the utility of animal movement characters in phylogenetic analysis even though the examples include a wide variety of taxa and cover an array of behavioural phenomena (Table 1). Successful use of animal movements in phylogenetic analysis requires two steps. First, one must make a detailed account about how an organism behaves during a behavioural repertoire. This will provide an understanding of all of the movements and actions an individual makes when performing a particular behavioural repertoire (see MILLER 1988 for detailed methodology). A lack of movement is also important and should be included in any analysis. Thus, a complete description of the feeding repertoire of a trap door spider, for example, should not only contain information about detailed movements of an individual during prey capture, but also information such as the

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orientation and location of the spider within the trap, and the orientation of its limbs while the individual is waiting. Reproductive and building behaviours are typically preferred (e.g., Table 1), but there is no reason to assume that other behaviours (e.g., feeding) cannot be studied in a similar fashion. The second step involves the study of other closely related species in a similar manner. Phylogeny reconstruction necessarily requires the comparative study of similar behaviours in order to discover shared derived character states. The comparative approach also aids in the description of behavioural repertoires because some phylogenetically informative movements may go undetected until some variation of the movement is observed in another taxon. As such, observation of multiple taxa typically reveals aspects of behaviour that had previously gone unnoticed (see MCLENNAN et al. 1988, PRUM 1990, PATERSON et al. 1995, KENNEDY et al. 1996, STUART & HUNTER 1998 for examples of this methodology). In order to use animal movement traits as phylogenetic characters there must be a consistent definition of a ‘behavioural unit’ so that all ethologists follow the same guidelines (WENZEL 1992). PROCTOR (1996) suggests that one reason for the limited use of behaviour in phylogenetic studies is the difficulty in delimiting characters. Her example is that of one observer recognizing three distinct behaviours in fish, ‘mouth gape’, ‘bow’ and ‘tail fan’, whereas another considers them to be one action: ‘fanning tail while bowing with open beak’. In order to recognize character states effectively it is necessary to study a group of closely related species. If after studying 20 species of fish, three species performed all three behaviours in the same order and none performed any of the solitary behaviours, then in the example provided above, one should consider ‘fanning tail while bowing with open beak’ as one character state. However, if certain species performed only ‘mouth gape’, then this character state should be recognized. A behavioural unit, therefore, is any behavioural trait shared by two or more taxa (WENZEL 1992).

Quantitative information Many behavioural studies concentrate on gathering quantitative information and each of the three types of behaviour discussed above have observable quantitative components. A behavioural category, such as aggressive behaviour, can be quantified by determining the frequency of aggressive bouts for individuals of a given species. In a trait that elicits a response, such as the species of prey captured, one can count the number of prey captured or the rate of prey capture. For specific movement information, each behavioural unit can be counted or timed; for example, the length of time for each building stage during black fly cocoon spinning (STUART & HUNTER 1998). There is potential difficulty in determining the homology of quantitative traits because their homology is dependent on the homology of the type of behaviour (as discussed above) being quantified. Thus, the number of times, or length of time that an animal behaves is only potentially homologous if the behaviour being performed is first shown to be homologous. Consider, for example, black fly larval cocoon spinning behaviour (see STUART & HUNTER 1995, 1998). Each building stage is characterized by a specific pattern of silking and a method of moving the head from the lateral surface of one side of its body to the other (i.e., method of crossing); both of which can be quantified (e.g., number of silk strands laid down per stage and number of times an individual crosses per stage). To demonstrate the dif-

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ference in assessing homology of these two quantitative traits we use the first stage of spinning, the ‘initial structure’ stage, as an example in three species of black fly, Prosimulium fuscum, Simulium venustum and Ectemnia invenusta. During this stage, larvae of all three species cross their head from one side of their body to the other by straightening their body and moving in an arc across to the other side. When optimized onto a phylogeny, this method of crossing is homologous; therefore, the quantitative information (e.g., number of crosses per stage) is potentially homologous. There are, however, two different methods of silking during the initial structure stage; transverse silking (i.e., larvae place strands perpendicular to the longitudinal axis of the resting larvae) performed by P. fuscum, and longitudinal silking (i.e., larvae place strands parallel to the longitudinal axis of the resting larvae) performed by S. venustum and E. invenusta (STUART & HUNTER 1998). Since the method of silking is not homologous among the three species, the quantitative information (e.g., number of strands per stage) cannot be considered homologous. Quantitative traits are potentially homoplasious, particularly across a broad range of taxa, because there is typically sufficient genetic variation within populations to permit evolution of the range of behavioural variation observed (FOSTER 1999). Therefore, shifts in the frequency of expression of behavioural traits could be common. However, it is currently difficult to assess amount of homoplasy in quantitative traits because they are rarely associated with known behavioural homologs. If animal movement or traits that elicit a response are shown to be homologous from a phylogenetic analysis, then quantitative information becomes valuable phylogenetic information (see discussion in previous section). KOREF-SANTIBAÑEZ (1972) performed an analysis of both qualitative and quantitative aspects of courtship behaviour in the semispecies of Drosophila paulistorum. Qualitative aspects of the animal movements were described in detail; the courtship elements and their sequence were similar for all semispecies except for one trait termed “shaking vibration” in males (very rapid vibrations of both wings which hardly leave the horizontal position), which did not occur in two semispecies. The other courtship traits (e.g., orientation, tapping vibration, scissoring), which were qualitatively similar, were counted, timed and compared among the semispecies. Although no phylogeny was reconstructed with these data, each semispecies had a characteristic courtship pattern based on relative frequencies of the courtship elements, and thus these data could potentially be used in phylogeny reconstruction.

IMPLICATIONS

Many misconceptions about the use of behavioural data in phylogenetic analyses occur because the term ‘behaviour’ applies to a variety of phenomena that are not equally applicable for understanding genealogical relationships. Although any observable trait, providing that it is heritable and variable, can theoretically be used as a character in a phylogenetic analysis, it seems prudent to be aware of the expectations and limitations of different behavioural types before they are included in a phylogenetic analysis. It is also important to differentiate the behavioural types and their respective expectations when assessing the phylogenetic usefulness of ‘behaviour’ in general. Some authors believe that behavioural characters are more labile and subject to homoplasy than are morphological characters (e.g., ATZ 1970, WCISLO 1989,

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WEST-EBERHARD 1989, HUNTINGFORD et al. 1994); whereas others assert that there is no reason to assume a priori that behaviour is any more subject to convergence than are other kinds of characters (e.g., LAUDER 1986, MCLENNAN et al. 1988, WENZEL 1992, DEQUEIROZ & WIMBERGER 1993, WIMBERGER & DEQUEIROZ 1996). We believe that both sides may be correct because the behavioural lability may largely depend on the type of behaviour studied. Although single studies do not tend to present data from all types (i.e., behavioural categories, reaction stimuli, animal movements and quantitative), certain trends are noticeable. Studies aiming to address adaptation level phenomena tend to use the presence or quantification of behavioural categories (e.g., presence or absence of cannibalism; intensity of aggressive behaviour) or reaction stimuli traits; these studies tend to find plasticity in behaviour (e.g., ARNOLD 1981, 1992; RIECHERT 1986; HUNTINGFORD et al. 1994; FOSTER 1995; FOSTER et al. 1996). For example, FOSTER et al. (1996) noted that isolated stickleback populations divide into limnetic and benthic sub-populations that have certain morphological and behavioural characteristics. Comparisons among populations suggested that adaptive change and homoplasy of behavioural phenotypes might be very common. The behavioural characteristics used by FOSTER et al. (1996) are either presence of behavioural categories (e.g., presence or absence of sneaking and cannibalism), or quantified behavioural categories (e.g., amount of boldness, conspicuousness of courtship). Similarly, HUNTINGFORD et al. (1994) studied adaptive variation in antipredatory behaviour in three-spined sticklebacks and showed that the intensity and nature of the antipredatory responses changed when predation regimes were varied. HUNTINGFORD et al. (1994) therefore used quantitative and reaction stimuli behaviours to determine trait adaptability. The inclusion of these traits into the construction of a phylogeny should be done with caution. Studies aiming to address questions of genealogical history tend to use the details of animal movements, and these studies find that behaviour is no more labile than other types of data (e.g., references in Table 1). For example, MCLENNAN (1993) documented 51 characters relating to the movements of sticklebacks during courtship behaviour and found that behavioural information actually provided a less ambiguous picture of relationships than did morphological data (MCLENNAN 1993, MCLENNAN & MATTERN 2001). Behavioural information can be a valuable source of information for understanding genealogical relationships among taxa and there is no reason for it to be avoided by systematists. If one is interested in using behavioural characters to reconstruct a phylogeny, we recommend using the following order of behavioural types: (1) animal movements; (2) quantitative components (providing that the animal movements are homologous); (3) reaction stimuli traits; (4) behavioural categories. Describing qualitative aspects of animal movements in detail for a number of taxa have repeatedly produced phylogenies that are corroborated by other data, regardless of taxa and/or behaviour studied (Table 1). Therefore, gathering behavioural data for phylogeny reconstruction should begin with an ethogram detailing the specific movements of individuals while performing a given behaviour. Many species should be studied similarly, characters gleaned from this analysis and a phylogeny reconstructed. Then, if the initial analysis of animal movements produces polytomies (i.e., unresolved regions) in the phylogeny, or if one is interested in constructing phylogenies of populations within a species, quantitative information can be investigated. It is only appropriate to use quantitative information as phylogenetic characters when the behaviours being quantified are homologous. Thus, a qualitative analysis of behaviour must precede or coincide with a quantita-

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tive analysis. We suggest that reaction stimuli traits be used with caution and behavioural categories be avoided. Characters arising from analyses of animal movements are the most likely to produce phylogenies that concur with other types of data, but unfortunately, this information is rarely gathered. Although it is possible to gather quantitative information and document stimuli that elicit a response while studying animal movements, it is not possible to gather information about an animal’s movements without observing them directly. Thus, we propose that the construction of behavioural phylogenies involve, first, an analysis of animal movements and characters resulting from this data. Since other behavioural information can be gathered simultaneously, this may also be included, but one should consider the appropriateness of behavioural types independently. Many biologists have detailed knowledge of the behaviours performed by their study organisms and this information can be of significant value for understanding the evolutionary history of these taxa. We hope that this discussion encourages behaviourists to use their data to reconstruct phylogenies and phylogeneticists to use behavioural characters in phylogeny reconstruction.

ACKNOWLEDGMENTS We thank NSERC for PGSA and PGSB awards to A.E. Stuart and operating grants to F.F. Hunter and D.C. Currie. We thank C. Currie, L. Jesson, D. McLennan, J. Napolitano, J. Rock, L. Rowe and J. Wenzel for comments on earlier versions of this manuscript.

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