Elsevier

Zoology

Volume 111, Issue 4, 15 July 2008, Pages 260-278
Zoology

Structure and composition of the courtship phenotype in the bird of paradise Parotia lawesii (Aves: Paradisaeidae)

https://doi.org/10.1016/j.zool.2007.07.012Get rights and content

Abstract

Ethology is rooted in the idea that behavior is composed of discrete units and sub-units that can be compared among taxa in a phylogenetic framework. This means that behavior, like morphology and genes, is inherently modular. Yet, the concept of modularity is not well integrated into how we envision the behavioral components of phenotype. Understanding ethological modularity, and its implications for animal phenotype organization and evolution, requires that we construct interpretive schemes that permit us to examine it. In this study, I describe the structure and composition of a complex part of the behavioral phenotype of Parotia lawesii Ramsay, 1885 – a bird of paradise (Aves: Paradisaeidae) from the forests of eastern New Guinea. I use archived voucher video clips, photographic ethograms, and phenotype ontology diagrams to describe the modular units comprising courtship at various levels of integration. Results show P. lawesii to have 15 courtship and mating behaviors (11 males, 4 females) hierarchically arranged within a complex seven-level structure. At the finest level examined, male displays are comprised of 49 modular sub-units (elements) differentially employed to form more complex modular units (phases and versions) at higher-levels of integration. With its emphasis on hierarchical modularity, this study provides an important conceptual framework for understanding courtship-related phenotypic complexity and provides a solid basis for comparative study of the genus Parotia.

Introduction

Ethology is based on the principle that complex behaviors can be broken down into component parts or characters – i.e., the ‘structural’ units that constitute phenotype (Lorenz 1950; Tinbergen, 1950, Tinbergen, 1952; Thorpe 1951; Hinde 1953; Barlow, 1968, Barlow, 1977; Nelson 1973; Wenzel 1993). This view of behavior has well-defined goals coinciding with the broader structuralist (sensu Amundson 2005) research program that aims to explain form as a product of both ontogeny and phylogeny (e.g., Daanje 1950; Tinbergen 1951; Baerends 1958; Blest 1961; Lorenz, 1965, Lorenz, 1966; Huxley 1966; Thorpe 1966; Hodos 1976; Greene and Burghardt 1978; Prum 1990; Wenzel, 1992, Wenzel, 1993; Greene 1994; Kennedy et al. 1996; Slikas 1998; McLennen and Mattern 2001). Implicit in this view is the notion that behavior, like morphology and genes, is inherently modular – i.e., composed of quasi-independent parts that are differentially expressed across hierarchical levels (West-Eberhard 2003).

In a morphological context, modules are units of phenotype organization (Raff 1996; Schlosser 2002; West-Eberhard 2003; Eble 2005) that are often repeated (or recurrent) entities within a phenotype (Raff 1996; Prum and Dyck 2003). They are also the units of variation, i.e., the characters and homologs of comparative biology (Raff 1996; Wagner 1996; Eble 2005). Modules are important for evolution because their semi-autonomy allows them to be dissociated from other modular units (Raff 1996; West-Eberhard 2003) and recombined in ways that promote mosaic evolution (Raff 1996; Schlosser 2002; West-Eberhard 2003).

Likewise, the ‘natural units’ of behavioral organization are also semi-discrete and recurrent entities called fixed/modal action patterns, which are envisioned as distinct ‘packets’ with characteristic ‘morphology’ (Lorenz 1950; Barlow 1977; Wenzel 1993). These units are the characters and homologs of comparative ethology and it is their inherent modularity that allows us to identify them in the first place, to perform comparative studies, and use behavioral data for phylogenetic reconstruction.

Yet, the behaviors routinely identified by researchers are not explicitly conceptualized as modular per se. This is especially true for complex communicative behaviors (e.g., courtship displays), which are often described as a part of studies aimed at determining adaptive function. Although it may not be necessary to describe the structure and composition (i.e., the ‘anatomy’) of a behavior because its sub-components may not have adaptive functions apart from the integrated higher-level unit, it is critically important to do so if one intends to understand the macroevolutionary mechanisms through which a behavior arose and was modified through time. But in recent decades, behaviorists have been more interested in function instead of form, and as a result, behaviors, especially social displays, have not been routinely dissected and described in ways that emphasize structural and/or modular organization. Consequently, the concept of modularity has not permeated the study of behavior in the same way it has permeated the study of other aspects of phenotype even though it is widely evident as a biological phenomenon and theoretically consistent with traditional perspectives on behavioral organization and evolution (Lorenz 1950; Tinbergen, 1950, Tinbergen, 1952; Thorpe 1951; Hinde 1953; Nelson 1973; Barlow 1977).

However, by not considering behavioral modularity as such we are precluded from investigating the generality of this important biological concept. Applying an explicit modularity concept allows behavior to be viewed as a complex phenomenon connected to multiple levels and multiple scales in development and evolution (West-Eberhard 2003). It connects observations of the phenotype from one level (e.g., patterns of organization) with observations and theory at other levels (e.g., how those patterns emerge and change in ontogeny and evolution; Wagner 1996; Raff and Raff 2000; Prum and Dyck 2003). Furthermore, explicit recognition of ethological modularity greatly enhances the implicitly modular thinking of early ethology and gives classic ideas like ritualization a new context for re-evaluation. For example, is ritualization better understood as a modular process whereby a “genuine activity” is effectively duplicated so that the duplicated units are expressed in another context and subsequently diverge independently to become “derived activities” (Tinbergen 1952)? Without a modularity concept applied to behavior we may never know.

Researchers interested in the organization and evolution of ethological form must clarify what ethological modularity is and how it is identified. One approach involves a multi-step process in which initial hypotheses of modularity are validated through subsequent studies (Geeta 2003; Eble 2005). In this way, discovery of the modular units of phenotype is somewhat like the discovery of homology – i.e., ‘true’ developmentally integrated units (i.e., secondary modularity) are first proposed as putative modular units (i.e., primary modularity) and subsequently tested via other means (Geeta 2003). Yet, no matter how the modular units of behavior are ultimately validated, the initial step is the same: clear articulation of the units of behavior at the phenotypic level. This means putting rigor into the descriptive enterprise and working to represent behavioral phenotypes in ways that clarify structural organization and ethological form (Scholes, 2006, Scholes, 2008a).

In this paper, one in a series of four, I use a hierarchical approach (Scholes, 2006, Scholes, 2008a) to describe the structural organization and ethological form of the units comprising courtship ethology in Lawes’ Parotia, Parotia lawesii Ramsay, 1885 – a bird of paradise (Aves: Paradisaeidae) from the mid-montane forests of eastern New Guinea (Frith and Frith 1981; Pruett-Jones and Pruett-Jones 1990; Frith and Beehler 1998). Birds of paradise in general, and species in the genus Parotia in particular, are some of the best examples of extreme (and unusual) phenotypic complexity among birds (Scholes 2006). This complexity stems from the aspects of phenotype related to courtship and mating and is influenced by strong sexual selection resulting from a lek-mating system (Pruett-Jones and Pruett-Jones 1990; Frith and Beehler 1998). The evolution of courtship complexity within the birds of paradise has given rise to tremendous disparity in courtship-related form among lineages. Explaining the origins and evolution of this disparity is important for understanding the evolutionary story behind this unique radiation, but it is also important for the broader goal of understanding the role of sexual selection in large-scale phenotypic change.

The goal of this paper is to identify the modular units of behavior at the phenotypic level (i.e., primary modularity) and describe hierarchical organization in a way that can serve as a basis for ongoing comparative study of the evolution of courtship-related form in the genus Parotia (Scholes, 2006, Scholes, 2008a). To accomplish this, I devise a conceptual model of phenotype organization that represents a complex aspect of phenotype. Behavioral units described here are identified using criteria similar to those used for decades (Whitman 1899; Daanje 1950; Baerends 1958; Tinbergen 1959; Greene and Burghardt 1978; Prum 1990; Wenzel 1992), but within a modern technological (e.g., vouchered video) and conceptual (e.g., hierarchical modularity) framework. These criteria include the specific arrangement of constituent parts within behavioral sequences, the recurrence of the same set of elements in space or time, and the temporal or spatial discreteness of components relative to similar units.

Finally, because of the precedent set in recent years, it should be pointed out that this study does not assess inter-individual variation in performance quality and/or its relationship to mating success (i.e., adaptive function). Rather, this study is meant to define and illustrate the components of courtship ethology and describe their relationships in a way that clarifies structural organization and ethological form. Results describe the distinctive modal properties of each behavior (as in “modal action patterns” of Barlow 1977), that is, the central characteristics that make a given behavior recognizable despite some individual differences in performance. The description of ethological form presented here is intended to be a comprehensive starting point for inter-specific comparative study that can be amended and modified when or if new data become available; it is also intended to clarify thinking about hierarchical modularity in complex behavioral phenotypes. Nevertheless, by comprehensively identifying the components of phenotype used in the context of courtship, these data may also prove useful as a baseline from which inter-individual variation can be measured in the future when trying to assess the selective mechanics and evolutionary implications of female choice – a critically important aspect of evolution in this group of birds (Pruett-Jones and Pruett-Jones 1990) not addressed in the present study.

Section snippets

Materials and methods

Courtship was studied near Crater Mountain in Eastern Highlands Province, Papua New Guinea (Fig. 1). The study area was 6 km north of the Herowana village airstrip at approximately 1500 m above sea level (06°36.120′S, 145°11.649′E). Fieldwork took place 13 November–10 December 2000 and 12–23 December 2001. Local assistants were employed to find terrestrial display territories and build observational hides. Video recordings were made from six focal display territories. Recording of unmarked birds

Display courts and leks

Of the nine courts examined, all were located on relatively flat portions of gently sloping ridges. They were irregular in shape and varied in size from less than 1 m2 to approximately 2 m2. They were found among relatively open areas of forest undergrowth, and not among shrubby thickets as observed in Parotia wahnesi (Scholes 2008a). The court floors were cleared of vegetation and all had at least one horizontal or sloping branch spanning the central part of the court that was used as a perch

Discussion

Since the beginning, ethologists have broken down complex behaviors into semi-discrete sub-components as a routine part of the comparative study of behavioral form. The ability to do so implies that behavior, like morphology and genes, is inherently modular and that ethological organization and evolution should be studied within a conceptual framework that takes modularity into account. Yet, as pointed out in the introduction, the behaviors routinely identified by behaviorists are not typically

Conclusions

Does describing the units of courtship behavior and terming them modules make them fundamentally different from the behavioral units described in the past? The simple answer is no. The biological reality of the units is the same regardless of what we call them (modal action patterns, characters, modules, etc.). Nevertheless, conceptualizing the ethological units that make up a complex phenotype as modular is critically important because it enhances the way we understand behavioral organization

Acknowledgments

Fieldwork was funded with research grants from the Wildlife Conservation Society (WCS), the Pacific Biological Foundation, and the National Geographic Society. I thank A. Mack, D. Wright, and the WCS Papua New Guinea Program for valuable logistical, financial, and moral support while doing fieldwork. I thank B.W. Benz for assistance in the field in 2001. Thanks to R. Prum, T. Peterson, K. Bostwick and two anonymous reviewers for improving the manuscript. I thank B. Clock at the Cornell

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