ANIMAL BEHAVIOUR, 1998, 56, 1044–1048 Article No. ar980874
Hierarchical patterns of covariance between morphological and behavioural traits MARGARET B. PTACEK & JOSEPH TRAVIS
Department of Biological Science, Florida State University (Received 15 January 1998; initial acceptance 1 April 1998; final acceptance 4 May 1998; MS. number: AS-1208R) attempting to insert the gonopodial tip into the female’s gonopore. This behaviour has no signal function, and there are no countersignals directed from the female towards the male. Farr (1989) contends that this behaviour cannot be considered a form of display. A second behaviour, termed a courtship display, is exhibited by a subset of poeciliid species. All poeciliid courtship displays are visual and involve a combination of stereotyped swimming motions and fin postures performed by males towards females in an attempt to elicit female cooperation in mating (Farr 1989). Rosen & Tucker (1961) note that in poeciliid species that show courtship display behaviours, stereotyped male courtship displays and female acceptance postures precede copulation. Most or all species that show courtship display behaviours also show frequent gonopodial thrusting. The fundamental observation of the interspecific pattern was made by Rosen & Tucker (1961) in their analysis of behavioural and morphological variation in several poeciliid species. They suggested that there was a negative association between male courtship display behaviour and relative length of the gonopodium (gonopodium length adjusted for variation in male body size). They found that, of the taxa they studied, those with long gonopodia (gonopodial length greater than one-third of body length) did not incorporate courtship display behaviour, or mouth or body contact during precopulatory interactions. Those taxa with short gonopodia (gonopodium less than one-third of body length) did perform courtship displays and made mouth or body contact. Their explanation for this pattern was predicated on the assumption that a long gonopodium was the plesiomorphic condition. While Rosen & Tucker offered no hypothesis for the origin of the short gonopodium, they suggested that courtship displays and less reliance on gonopodial thrusts evolved to increase the effectiveness of the short gonopodium that was already present in certain genera such as Gambusia and Poecilia. In particular, the need to properly position the shortened gonopodium drove the evolutionary modification of pectoral and pelvic fins in males for greater manoeuvrability (see also Hubbs & Reynolds 1957; Peden 1972); courtship displays evolved to elicit female cooperation so that males could obtain the relatively longer time needed for
hen correlations among a set of traits within a species strongly resemble the correlations among these same traits across species, it is tempting to explain the origin of the interspecific pattern by the same mechanisms that are observed to maintain the intraspecific pattern (Travis 1994a). In this note we suggest that it is necessary to consider a variety of hierarchical levels of covariation among traits before drawing that parallel. While other workers have made similar points about how phylogenetic information can help refine hypotheses for the evolution of broad interspecific associations among traits (Carothers 1984; Maddison 1990 cited in Sillen-Tullberg 1988; Cooper 1995; McPeek 1995), we ask whether micro-evolutionary maintenance processes can be used to infer the origin of macro-evolutionary patterns within a group. The question is an appropriate one for many classes of characters, but we feel it particularly important when behavioural traits are involved because of the interest in the way in which behavioural variation can drive the evolution of other types of traits (Wcislo 1989; West-Eberhardt 1989; Basolo 1995). Additionally, results from intraspecific studies of behavioural variation have been used to interpret broad interspecific correlations (e.g. Basolo 1990; Losos 1990; Emerson 1991; Reynolds et al. 1993; Morris & Ryan 1996). We use poeciliid fish as our example. In particular, we examine the positive association between body sizeadjusted gonopodium length and reliance on forced insemination. The gonopodium is the modified anal fin used by males of all poeciliid species to place spermatophores on or within the female’s genital opening for internal fertilization. We ask whether it is reasonable to interpret the current selective forces maintaining this correlation among individuals within a population as reflective of the historical selective pressures that molded the interspecific association. All poeciliids observed to date perform a type of forced insemination attempt termed a gonopodial thrust. The male orients himself behind a female, brings the gonopodium to a forward position, and swims forward,
W
Correspondence: M. B. Ptacek, Department of Biological Sciences, Idaho State University, Pocatello, ID 83209-8007, U.S.A. (email:
[email protected]). 0003–3472/98/101044+05 $30.00/0
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1998 The Association for the Study of Animal Behaviour
COMMENTARIES 1045
successful copulation with a shorter gonopodium (see also Farr 1989). In this explanation, the short gonopodium mediated the subsequent evolution of the paired fins and the behavioural repertoire of courtship displays. Reynolds et al. (1993) revisited the association of gonopodium length and behavioural repertoire. They found a positive correlation between gonopodium length and rates of gonopodial thrusting among male guppies within a single population. They suggested that this association was consistent with the hypothesis that male guppies in that population were under selection to circumvent female choice and responded by increasing length of the gonopodium. From this observation they speculated that ‘. . .the selective processes occurring within guppy populations may be similar to those that have produced interspecific variation in mating behaviour and morphology.’ The question we address is not whether Reynolds et al. (1993) are correct about the action of selection within contemporary guppy populations; we think they are. Rather, we address whether the ‘evolutionary uniformitarianism’ implied by their statement about the usefulness of studying microevolutionary processes can be justified. We will show that it might be justified, but not in a way that Reynolds et al. (1993) could have anticipated. We will show that their explanation for the intraspecific correlation cannot account for the wellknown interspecific association, primarily because the association between long gonopodia and reliance primarily on gonopodial thrusting is looser and more variable among hierarchical levels than first appearances indicate. However we will suggest that their explanation may account for a pattern of covariation of which they could not have been aware. To begin, we review our current understanding of poeciliid systematics. In 1963, Rosen & Bailey published a systematic monograph on the family Poeciliidae. Their volume did not include a key to the genera or species, nor did it present definitions of, or relationships among subgroups using solely synapomorphic characters. While limited phylogenetic information exists for relationships among a few of the tribes within the subfamily Poeciliinae (mostly with respect to this subfamily’s position among the other subfamilies in the order Cyprinodontiformes: Parenti 1981; Meyer & Lydeard 1993), little attention has been paid to relationships among the tribes within this subfamily and their phylogeny is mostly unresolved (Parenti & Rauchenberger 1989). According to Parenti & Rauschenberger (1989), the subfamily Poeciliinae has two monophyletic supertribes, each supported by several synapomorphic characters, the monotypic Tomeurini and the Poeciliini. The supertribe Poeciliini consists of seven tribes, Poeciliini, Cnesterodontini, Scolichthyini, Gambusiini, Girardinini, Heterandriini and Xenodexiini, whose relationships are unresolved (Fig. 1). Although Rosen & Tucker (1961) discussed the association between long gonopodia and the absence of courtship displays at the generic level, the association is actually consistent at the levels of the supertribe and tribe. To demonstrate this, we updated Rosen & Tucker’s
Supertribe Poeciliini Poeciliini (4, 65) GT, CD; Short Cnesterodontini (4, 8) GT; Long Scolichthyini (1, 2) GT; Long Gambusiini (3, 55) GT, CD; Long, Short Girardinini (3, 11) GT; Long Heterandriini (5, 45) GT; Long Xenodexiini (1, 1) GT; Long Supertribe Tomeurini (1, 1) GT; Long
Other Cyprinodontiformes
Figure 1. Hypothetical tree based on our current understanding of the phylogenetic relationships among supertribes and tribes of the family Poeciliidae. There is support for the separation of Tomeurini as a monophyletic group (80–88% bootstrap values) outside of Poeciliini based upon the phylogenetic analyses of Meyer & Lydeard (1993). For further discussion, refer to the text. Numbers in parentheses refer to (number of genera, number of species). GT=presence of gonopodial thrusting, CD=presence of courtship display behaviours, Long=gonopodial length greater than one-third of total body length, Short=gonopodial length less than one-third of total body length.
compilation with Farr’s (1989) survey of mating behaviours in the family (Fig. 1). Courtship displays have been observed only in species of the Gambusiini and Poeciliini. All four genera of Poeciliini (Alfaro, Poecilia, Priapella and Xiphophorus) have short gonopodia and courtship displays have been observed in males of some, but not all, species of Poecilia and Xiphophorus. Of the three genera within the Gambusiini, Belanesox have short gonopodia and males perform courtship displays, the others (Gambusia and Brachyraphis) have species with both short and long gonopodia and the majority of species in each genus rely primarily on gonopodial thrusting, although limited levels of courtship display behaviours have been reported in some species of Gambusia (Rosen & Tucker 1961; Peden 1972). All species in the five remaining tribes have long gonopodia and do not exhibit courtship display behaviours (Farr 1989). Thus only in tribes with short gonopodia do males of certain species perform courtship displays, and therefore at the tribal level there is an association between long gonopodia and the absence of courtship displays and increased reliance on gonopodial thrusting (Fig. 1). It is unclear if the association is found among the genera within the two tribes that have taxa with courtship displays. Two of the three genera within the Gambusiini are known to show courtship displays in some of their species (Belanesox and Gambusia), but it is unclear if courtship display behaviours exist in the third, Brachyraphis; Farr (1989) suggests that some species will
1046 ANIMAL BEHAVIOUR, 56, 4
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Figure 2. Natural log (ln) of the length of the gonopodium plotted against log of the standard length, which is the measure of body length in fish, for males from three species of poeciliid fish. Symbols denote species identity as L=P. latipinna, M=P. mexicana, O=P. orri. Linear regressions were significant for P. latipinna (F1,28 =35.29, P
