Using phylogenies to study convergence: The case of the ant-eating mammals

Using Phylogenies to Study Convergence: The Case of the Ant-Eating Mammals'1

SYNOPSIS. Identifying when homoplasy is due to convergence requires confidence in trees and precise analysis of potentially convergent characters. Some features of mammals that eat mostly ants and termites are used as examples of convergence; the most speciose assemblages of these mammals are in the orders Xenarthra and Pholidota. My studies on cranial muscles in xenarthrans and pholidotans aim to 1) precisely describe the anatomy in ant-eating and non-ant-eating lineages, 2) assess variation among ant-eating lineages, and 3) compare the most derived conditions (in xenarthran anteaters and pholidotan pangolins). These data clarify the nature of morphological adaptation in ant-eating mammals, and when combined with accumulating phylogenetic studies, allow us to distinguish features that have evolved convergently from those that are variable but not correlated with diet. Interpreting the extreme similarity in anteaters and pangolins remains problematic due to lingering disagreement among phylogenetic hypotheses. Prevailing opinion favors interpretation of these similarities as convergent.

INTRODUCTION

There are two ways by which organisms can evolve similar features. They can inherit such features from a common ancestor, which results in their phylogenetic homology (Nelson, 1994). Alternatively, two or more lineages can independently evolve similarities after their divergence from a common ancestor. This is convergence. Convergence is seen in phylogenetic analyses as homoplasy, but homoplasy can also result from reversal of a character state to the primitive condition in one or more lineage (Brooks, 1996). Convergence in morphology can occur in general and superficial characteristics of organisms (as in the fusiform body shape of fishes and whales) but is more interesting when it occurs in specific structures that are topographic or topological homologues, i.e., the "same" structures as identified by positional and developmental criteria (Rieppel, 1994).

One example of convergence in specific and topographically homologous characters-often cited in textbooks (e.g., Eisenberg, 1981; Pough et al., 1989; Simpson and Beck, 1965; Vaughan et al., 1999)comes from mammals that specialize on ants and/or termites (myrmecophages) (Fig. 1). The difficulty imposed by trophic specialization on small, nutritionally poor and aggresive prey is thought to have necessitated the evolution of a stereotypical set of features that are adaptive for ant-eating (Griffiths, 1968; Redford, 1987). The most well known of these features is the slender, elongate and highly extensible tongue. This tongue is hypothesized to allow rapid and deep penetration of prey nests and to provide surface area for the adherence of many prey items during each intrusion into the nest. Other presumably adaptive features include a dominant and especially sharp claw on the manus and robust forelimb flexor muscles for breaking into nests, stocky plantigrade hindlimbs anchored to a heavily fused pelvic girdle providing a solid base of support for forelimb activities, and thick integument, small pinnae and valvular nostrils to minimize susceptibility to attacking prey.

I have looked closely at this purported example of convergence, from the perspective of a morphologist particularly interested in the evolution of muscles in the mammalian feeding apparatus (Reiss, 1997a, b, 2000). Several questions arise during a critical analysis of this example. First, are we certain that the relevant taxa are unrelated and couldn't have inherited similarities from a common ancestor? The patterns of taxon interrelationships revealed by phylogenetic analysis allow homologous and homoplasious similarities to be differentiated, and only homoplasious similarities are candidates for convergence. Second, what are the specific morphological differences between ant-eating mammals and more trophically generalized mammals? Defining quantitative and qualitative features of the ant-eating tongue type is a first step in answering this question. Beyond that, unusual tongue morphology might coincide with unusual configurations in other components of the feeding apparatus, since the components of the mammalian feeding apparatus are known to function in a tightly integrated manner (Hiiemae, 2000). Comparative anatomical studies can document the extent of modifications in ant-eating mammals and enumerate the specific character states that are candidates for convergence. Finally, which of these character states are shared among the unrelated ant-eating taxa? Identifying which features are convergent in which taxa is necessary in order to formulate specific hypotheses about the causes of convergence. While convergence is traditionally ascribed to the action of natural selection on animals with similar ecological challenges, it can also result from shared phylogenetic and/or developmental factors that favor certain structural configurations out of the range of all imaginable morphologies (Wake, 1991). Clarifying the roles of these processes in generating convergent morphology requires that we first define the phenomenon.