© 2001 by The Society for Integrative and Comparative Biology
Using Phylogenies to Study Convergence: The Case of the Ant-Eating Mammals1
1 Department of Biological Sciences, Humboldt State University, Arcata, California 95521
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 SYNOPSIS INTRODUCTIONXENARTHRA AND PHOLIDOTAOTHER MAMMALIAN MYRMECOPHAGESEXPLAINING PATTERNS OF...CONCLUSIONSReferences |
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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.
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INTRODUCTION |
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SYNOPSISINTRODUCTIONXENARTHRA AND PHOLIDOTAOTHER MAMMALIAN MYRMECOPHAGESEXPLAINING PATTERNS OF...CONCLUSIONSReferences |
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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.
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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.
The mammalian orders Xenarthra and Pholidota contain the most speciose assemblages of myrmecophages—mammals with diets that consist of at least 90% ants and/or termites (Redford, 1987)—so it is here that I have focused my own studies. I will first address my three questions with respect to ant-eating Xenarthra and Pholidota, and then expand my discussion to include what is known about other mammalian myrmecophages.
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XENARTHRA AND PHOLIDOTA |
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SYNOPSISINTRODUCTIONXENARTHRA AND PHOLIDOTAOTHER MAMMALIAN MYRMECOPHAGESEXPLAINING PATTERNS OF...CONCLUSIONSReferences |
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What do we know about the phylogenetic relations of Xenarthra and Pholidota? Both taxa are placental or eutherian mammals, but their relationships to other eutherians continue to be a source of discussion. The Xenarthra, found only in the New World, is a trophically diverse group (Montgomery, 1985a
). It contains the myrmecophagous anteaters (Family Myrmecophagidae), the armadillos (Family Dasypodidae), some species of which are myrmecophagous (Redford, 1985, 1987), and the sloths (Families Bradypodidae and Megalonychidae), which are specialized folivores. The Xenarthra is probably monophyletic (Engelmann, 1978, 1985; Van Dijk et al., 1999) and is probably the basal clade of extant eutherian mammals (Honeycutt and Adkins, 1993; Novacek, 1993; Novacek and Wyss, 1986; Shoshani, 1986) (Fig. 2). In contrast with the Xenarthra, the Old World Pholidota is not trophically diverse and contains only the myrmecophagous pangolins, or scaly anteaters (Patterson, 1978). It is uncontroversially monophyletic (Gaudin and Wible, 1999) and has been suggested to be a) most closely related to the anteaters within the Xenarthra (Engelmann, 1978; Norman and Ashley, 1994; Reiss, 1997a), b) the sister taxon of the Xenarthra (Honeycutt and Adkins, 1993; McKenna, 1992; Novacek, 1993; Novacek and Wyss, 1986; Novacek et al., 1988), or c) most closely related to the Carnivora (Honeycutt and Adkins, 1993; McKenna, 1987; Murphy et al., 2001) (Fig. 3).
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Attempts to resolve the relationships of Xenarthra and Pholidota to other eutherian mammals have not yet been exhausted. Taxonomic representation within each order has been thin in most molecular studies, and there has as yet been no analysis that combines morphological and molecular data in a single data matrix (though a recent supertree analysis included both molecular and morphological source trees (Liu et al., 2001)). Of the three hypotheses, that which places Pholidota within Xenarthra has little support. Most morphological data sets support the sister-group relation of Xenarthra and Pholidota, and their basal position among eutherians. This leads to three possible interpretations of similarity between anteaters and pangolins—retention of primitive eutherian features, inheritance from a myrmecophagous or insectivorous common ancestor of Xenarthra and Pholidota, or convergence. On the other hand, molecular data sets tend to support the sister-group relationship of Carnivora and Pholidota, usually with Xenarthra as basal for Eutheria. According to this hypothesis, similarities between anteaters and pangolins are either primitive or convergent. By looking at the characters in question in a broad phylogenetic context we can distinguish between these alternative interpretations and reveal which characters have, in fact, evolved convergently.
Let's turn to what is known about the anatomy of the feeding apparatus in Xenarthra and Pholidota. These curious animals have excited the interest of comparative anatomists for centuries. For example, Pouchet and Owen published beautiful descriptions of cranial anatomy in giant anteaters in the 1800s (Owen, 1862; Pouchet, 1867), and in modern times, Chan's study of the pangolin tongue (Chan, 1995) and Naples' work on sloth cranial anatomy (Naples, 1982, 1985a, b, 1986) stand out. Yet despite these and other studies (Cheng, 1986; Dingler, 1964a, b; Doran and Allbrook, 1973; Edgeworth, 1914, 1916, 1923, 1935; Ehlers, 1894; Frick, 1951; Friend, 1982; Hoever, 1910; Imai, 1978; Kubota et al., 1962a, b; Kühlhorn, 1939; Nene, 1978; Saban, 1968; Sonntag, 1923, 1925a; Storch, 1968; Uekermann, 1912; Windle and Parsons, 1899) I found that the necessary data for a complete character analysis were not available. Some studies were limited in scope, focusing on only one portion of the feeding apparatus, usually the tongue. These would not enable me to assess the extent of anatomical differences from a generalized condition throughout the entire feeding apparatus, nor enable me to compare the extent of similarities among different ant-eating taxa. Prior work was also plagued by inconsistencies in muscle nomenclature. If innervation of these sometimes unusually positioned muscles is not documented, determining topographic homology between taxa is difficult, and hypothesizing topographic homology is a necessary prelude to defining characters. Finally, some relevant taxa were well studied but others had not been examined. For example, whereas the above-mentioned monographs on giant anteaters are quite complete and have been available for over 100 yr, little was known for other species of xenarthran anteaters.
To remedy these problems and enable a phylogenetic analysis of feeding apparatus characters to be conducted I performed my own series of dissections of xenarthran and pholidotan taxa. I included all muscles associated with the jaws, tongue and hyoid, palate, and pharynx (Table 1). I paid close attention to topographic homology, identifying muscles by attachments and/or innervation, and named muscles accordingly. I used each of 27 cranial muscles as characters and for each defined character states that reflected qualitative differences in gross anatomy, i.e., major differences in origin, insertion, position, etc. (Table 2). Finally, I sampled extensively within Xenarthra and Pholidota. I looked at three of the four anteater species; three of seven pangolin species including animals from both the Asian and the African species groups; an ant-eating and a non-ant-eating armadillo (identified according to Redford, 1987); and a species from each of the two extant sloth genera (Table 3). To assess character polarities I added the domestic dog, Canis familiaris, to represent a relatively generalized eutherian (Evans and Christensen, 1979), and used the common opposum, Didelphis marsupialis, as an outgroup (Edgeworth, 1935; Ellsworth, 1976; Hiiemae, 1976; Saban, 1968). I used PAUP* 4.0b4a (Swofford, 1998) to generate a shortest tree from the resultant data matrix (Table 4) and I used MacClade (Maddison and Maddison, 1992) to map character states onto this tree and onto alternative trees.
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The dissections made it clear that the similarities between anteaters and pangolins go far beyond having a long and thin tongue; they are detailed and extensive (Reiss, 1997a, b, 2000
). Many muscles are qualitatively different from the typical eutherian condition. The jaw adductor muscles, masseter and temporalis, are small and architecturally simple. Virtually all tongue muscles show some modification, but in particular, the hyoglossus and sternohyoideus are fused to form a long and continuous strap, the sternoglossus, that arises from the sternum, is free from the hyoid apparatus, and makes up the bulk of the tongue. The mylohyoideus and stylopharyngeus, unusually, contribute transverse fibers to the soft palate. And finally, the pharynx contains a novel muscular sheath comprised of mylohyoideus and posterior digastric that surrounds the pharyngeal segment of the tongue. The main differences between anteaters and pangolins are that the soft palate extends caudally into the neck in anteaters, and the muscular sheath surrounding the tongue is better developed in pangolins, in which it has been dubbed the glossal tube (Chan, 1995). All of these muscle character states differ from the condition seen in the opossum, and also differ from the likely primitive condition for eutherians (inferred by assessing the most widely distributed character states among eutherians), suggesting that these unusual anteater and pangolin features are derived.
Not surprisingly, then, phylogenetic analysis of these muscle data yields a shortest tree that places anteaters and pangolins as sister taxa within Xenarthra (Reiss, 1997a) (Fig. 4). This particular hypothesis suggests that Xenarthra as currently defined is paraphyletic, but this is discordant with the bulk of other character data (e.g., Rose and Emry, 1993; Szalay and Schrenk, 1998), and phylogenetic studies (e.g., Engelmann, 1985; Gaudin, 1995; Gaudin and Branham, 1998; Murphy et al., 2001) that support xenarthran monophyly. Moreover, the strong signal for a monophyletic Pilosa (anteaters and sloths) within the Xenarthra is also not retrieved in this analysis. These irregularities are expected artifacts of running an analysis with limited data, all from a single functionally integrated system. Indeed, this is a general problem with using parsimony to retrieve phylogenies in systems where extensive convergence has occurred (e.g., see Pettigrew, 1991, and responses to his study in the same issue). More realistic scenarios for character evolution result from mapping these character states onto trees built from more extensive data sets, i.e., those that reflect the three hypotheses discussed earlier (Figs. 4–6).
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The tree in which pangolins and anteaters are sister taxa within a typically structured Xenarthra (Fig. 5) is 4 steps longer than the shortest tree. The ingroup is supported by a single character state change, the freeing of sternohyoideus from the hyoid apparatus (character 26), though the fate of this muscle in the terminal taxa varies. In all xenarthrans, sternohyoideus attaches to the anterior digastric (5, but not mapped because its reconstruction is ambiguous) instead of to the hyoid, resulting in a compound sternomandibularis. In pangolins, sternohyoideus attaches to the hyoglossus (12) forming a compound sternoglossus. These conditions coexist in anteaters, in which the sternohyoideus is completely divided longitudinally (inferred from the presence of two straps innervated by the hypoglossal nerve in addition to a typical sternothyroideus). The anteater-pangolin clade shares a number of derived character states including simplification of the temporalis (2), and perhaps also the masseter (though reconstruction of this character is ambiguous), mylohyoideus and stylopharyngeus fibers in the soft palate (6; 13), attachment of the lingual portion of palatoglossus to the hyoid (20, though this character changes again in Tamandua), contribution of genioglossus to a band of muscle encircling the tongue (21), loss of the styloglossus (22), and the freeing of the hyoglossus from the hyoid (23, though this changes again in the Tamandua-Myrmecophaga clade). Homoplasy among ant-eating forms is limited to jaw adductor reduction (1; 2) shared by the ant-eating armadillo Dasypus and the anteater-pangolin clade, and a robust mandibuloauricularis shared by Dasypus and anteaters (10). Other homoplasy includes a single-bellied lateral pterygoid (4) that pangolins share with Canis, and a simplified stylopharyngeus (13) that Choloepus shares with Canis. The condition of the lateral pterygoid varies in other eutherians (Saban, 1968
), but as far as I know, the simplified stylopharyngeus is ubiquitous and can thus be considered a synapomorphy for Epitheria (Eutheria exclusive of the basal clade) that is convergently derived in the sloth genus Choloepus.
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Cranial muscle characters states mapped onto either of the alternative trees requires an additional 12 steps compared with the shortest tree. If Pholidota is placed as the sister group to the Xenarthra (Fig. 6) the ingroup content is the same and it is still supported by a change in the sternohyoideus (26). Most tongue, palatal and pharyngeal muscle character state changes are now homoplasious between pangolins and myrmecophagids. Additional homoplasy is seen in the jaw adductors of Dasypus and pangolins (1; 2), the mandibuloauricularis of Dasypus and anteaters (10), and the palatinus (19) of sloths and pangolins. Stylopharyngeus simplification (13) remains a putative synapomorphy for Epitheria on this tree. On the tree with Pholidota as the sister taxon to Canis (Fig. 7) most of the above-mentioned jaw, tongue, palatal and pharyngeal characters are, again, homplasious. What changes on this tree is that changes for several characters of interest, i.e., temporalis (2), stylopharyngeus (13), styloglossus (22) and sternohyoideus (26), can not be unambiguously reconstructed. These ambiguities are mainly attributable to using a single genus, Canis, to represent eutherians, and if we factor in what is known about the cranial anatomy of other eutherians, these characters are added to the list of homoplasious transformations. On the other hand, the presence of a single-bellied lateral pterygoid (4), which was homplasious on the previous trees, becomes a synapomorphy for the Manis-Canis clade. As mentioned above, this character is variable among eutherians and, hence, is a questionable epitherian synapomorphy.
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In sum, even though the phylogenetic interrelationships are uncertain, this exercise has revealed some noteworthy information about cranial muscle evolution in these taxa. First, most of the specializations in the feeding apparatus of myrmecophagous xenarthrans and pholidotans cannot be interpreted parsimoniously as primitive characters retained from a common ancestor. They are derived character states. They can be interpreted as derived features of an anteater-pangolin clade or as convergent, depending on which tree one prefers. Other data sets deem an anteater-pangolin clade unlikely, supporting the traditional interpretation of character convergence. The present analysis makes it clear how deep this convergence is.
A second result of this analysis is that myrmecophagous armadillos, represented here by Dasypus, share few specializations with the other myrmecophages. Only reduced jaw adductors and a robust mandibuloauricularis (which may function as a jaw retractor) are similar between Dasypus, anteaters and pangolins. Whether other members of the myrmecophagous armadillo clade are significantly different from Dasypus remains to be seen, and further taxon sampling within armadillos would be useful.
Finally, though extensive character convergence is implied on both alternative trees, there are differences in character evolution scenarios depending on whether pholidotes are allied with xenarthrans or epitheres. The unusual muscular composition of the soft palate, and the muscles that have become free of the hyoid to fuse in series, are two particularly striking features of anteater and pangolin cranial anatomy. If Xenarthra and Pholidota form a clade, one can look for antecedents of these features in the common ancestor of the clade. If pholidotes are not closely related to xenarthrans, one needs to look for more general causes of convergence. These ideas are discussed more fully below, after we consider anatomical specializations in the other mammalian myrmecophages.
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OTHER MAMMALIAN MYRMECOPHAGES |
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SYNOPSISINTRODUCTIONXENARTHRA AND PHOLIDOTAOTHER MAMMALIAN MYRMECOPHAGESEXPLAINING PATTERNS OF...CONCLUSIONSReferences |
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Expanding the discussion to consider other ant-eating taxa, we must first address the phylogenetic question—are we certain that these taxa are unrelated? The answer here is a resounding yes. Despite ongoing controversies regarding mammalian higher-level interrelationships, it is fairly certain that neither echidnas (Prototheria), numbats (Metatheria), aardwolves (Carnivora) nor aardvarks (Tubulidentata) are the sister group of any other mymrecophagous taxon, including anteaters (Xenarthra) and pangolins (Pholidota) (Fig. 1). Even if pangolins are the sister group of carnivores, aardwolves are well nested within Carnivora in the family Hyaenidae. Unfortunately, information on the condition of feeding apparatus muscles in ant-eating taxa outside the Xenarthra and Pholidota is incomplete. Most of the information I have found is from Schulman's treatise (Schulman, 1906
) on the echidna Tachyglossus, Frick (Frick, 1951), Sonntag (Sonntag, 1925a, b) and Shoshani's (Shoshani, 1993) work on aardvarks, and Richardson's work on aardwolves (Richardson, 1985, 1987). For the present purpose, these studies are plagued by the same shortcomings as were the previously available xenarthran and pholidotan studies. Nevertheless, a review of this literature clearly reveals one important point. There is a gradation of specializations among ant-eating taxa (Fig. 8). Aardvarks and aardwolves have a fairly typical eutherian feeding apparatus, though they both have simple teeth lacking enamel. Ant-eating armadillos represent an intermediate grade in that not only their teeth but also their jaw adductor musculature is reduced. Finally, anteaters and pangolins represent the extreme case with no teeth, reduced jaw adductors, and the anomalous conditions of the tongue, palate and pharyngeal muscles already discussed. Echidnas appear to be close to the anteater and pangolin extreme.
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As an example of this gradation, consider the tongue, long the classic example of convergence and a case where the detailed anatomy is clear in all taxa. In a typical eutherian mammal, the tongue is squat and chunky, fills much of the oral cavity and oropharynx, and is comprised of several extrinsic muscles (usually genioglossus, styloglossus, palatoglossus and hyoglossus), which arise from various cranial skeletal surfaces and connective tissues, including the basihyal bone of the hyoid apparatus. Aardvarks and aardwolves have this typical eutherian construction. The ant-eating armadillo has a fairly typical tongue with the exception that it is unusually thin and elongate (Fig. 9a). In the echidna, anteaters, and pangolins, there are qualitative differences in tongue construction. In the echidna, hyoglossus and sternohyoideus partially maintain their usual attachment to the basihyal bone, but portions of each are fused in series with one another forming a compound sternoglossus that runs from sternum to tongue and bypasses the hyoid apparatus ventrally (Fig. 9b). In anteaters and pangolins, the hyoglossus and sternohyoideus are completely detached from the hyoid and the body of the tongue is formed wholly of the genioglossus and the compound sternoglossus (Fig. 9c, 9d). In all three of these taxa, other tongue muscles are either absent (e.g., styloglossus) or do not enter the tongue (e.g., palatoglossus). Given the detailed similarities present to a greater or lesser degree among unrelated myrmecophages, how do we explain them?
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EXPLAINING PATTERNS OF CONVERGENCE |
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SYNOPSISINTRODUCTIONXENARTHRA AND PHOLIDOTAOTHER MAMMALIAN MYRMECOPHAGESEXPLAINING PATTERNS OF...CONCLUSIONSReferences |
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Explaining convergence leads inevitably to a consideration of the complementary roles of adaptation and constraint (Brooks, 1996
; Wake, 1991). Adaptationist "just-so" stories are fairly easy to come by, and form productive starting points from which to generate hypotheses about the function of specific features. However, phylogenetic history and shared developmental pathways can also channel morphological variation into particular configurations which must certainly function, but for which the raison d'être is not adaptation. Through a combination of anatomical and phylogenetic approaches I have documented two patterns in the evolution of myrmecophage cranial muscles. First, I have identified particular character states as convergent. Second, I have identified particular taxa that show more extensive convergence (involving more characters) than others. How can we explain these patterns?
With respect to the extensive character convergence seen between anteaters and pangolins, we can ask what it is about these particular taxa that might have fostered the evolution of such extreme morphological specialization. From an adaptationist point of view, if these taxa are more morphologically specialized than other myrmecophages, they must also be more ecologically and/or behaviorally specialized (why these adaptations are necessary is discussed below). There is some evidence to support this hypothesis. For most anteater and pangolin species, preference for ants and/or termites, preference for nest-site feeding, and foraging behavior involving nest break-in, a brief feeding bout, and then a move to another nest, are all well documented (Lubin et al., 1977; Montgomery, 1985b; Pagès, 1965, 1970). In contrast, recent work on a supposedly ant-eating armadillo suggests that its diet varies dramatically across seasons (Bolkovic et al., 1995), and this may be true for other armadillos as well. Also, the aardvark is reported to eat wild cucumbers in addition to ants and termites (Meeuse, 1963). The aardwolf is a undoubted termite specialist but it does not feed at nests, rather, it laps up exposed workers assembled along foraging trails (Richardson, 1987). Reports on the degree of trophic specialization in the long-beaked echidna Tachyglossus vary, but recent reports from Kangaroo Island suggest that they are generalized insectivores (Rismiller, personal communication), and the short-beaked Zaglossus is thought to be an earthworm specialist (Nowak, 1991).
There may also be phylogenetic constraints that can help explain the taxonomic distribution of specializations. For two of the three hypotheses of relationships (trees 5 and 6) anteaters and pangolins are found in a clade that is basal to other eutherians. One can ask whether the evolution of their particular specializations was facilitated by characteristics of the common ancestor of the basal clade that are different from the common ancestor of other eutherians, i.e., a uniquely derived feature of the basal clade or a retained primitive character that changes in the common ancestor of epitheres. Only two characters fit these criteria. Freeing of the sternohyoideus from the hyoid bone (26) is a synapomorphy of the basal clade, and one can speculate that this set the stage for the later evolution of compound muscles containing sternohyoideus fibers (i.e., sternoglossus and sternomandibularis). However, each of these compound muscles can be found outside of the basal clade, e.g., sternoglossus in nectar-feeding bats (Griffiths, 1982) and sternomandibularis in the hippopotamus (Herring, 1975). Alternatively, the primitive condition of the stylopharyngeus (13) is seen in the common ancestor of the basal clade. The stylopharyngeus (13) is a small slip of longitudinal fibers in epitheres, but its primitive condition is robust with both transverse and longitudinal fasicles. One can speculate that the primitive condition allows the later invasion of the soft palate by the transverse fibers. Of course, this scenario is complicated by homoplasy in the reduction of the stylopharyngeus, seen both in the sloth Choloepus and the epitheres. Finally, our third hypothesis of relationship, which places pangolins with carnivores, offers no obvious constraint scenario for any character. In sum, we can conclude that there is no evidence that phylogenetic constraints have facilitated or prevented the evolution of cranial muscle specializations for myrmecophagy.
Turning from an attempt to explain which taxa are the most convergent to the specific characters exhibiting convergence, we can again contrast adaptationist and constraint viewpoints. From an adaptationist point of view, we can ask the question "What is the functional significance of the specializations we see?" Reduced teeth and jaw adductor musculature are rather obviously correlated with the abandonment of mastication behavior. Bryan Patterson suggested that abandoning mastication is a way for a mammal to increase the speed of ingestion (Patterson, 1975). Speed of ingestion is presumably important because of the small size and low nutritional value of the prey (Redford and Dorea, 1984) as well as the rapidity with which prey defensive strategies are mobilized (Lubin and Montgomery, 1981, 1985b). The thin and elongate tongue is suggested to be a dexterous probe of the labyrinthine passages of prey nests—the more extensible it is, the more deeply the nest can be penetrated. Moreover, a thin and elongate tongue presumably has low inertia and this could also facilitate speed during excursion. The unusual musculature of the pharynx may aid in tongue elevation (since the usual tongue elevating muscles are lost or have been modified) and that of the soft palate may aid in the intra-oral management of live prey (e.g., preventing them from crawling into the nasopharynx).
To move beyond the limitations of just-so stories, these functional hypotheses all need to be tested. Unfortunately, experimental functional morphological studies in ant-eating taxa are almost completely lacking, as are field-based studies of natural feeding behavior. We do not know the kinematics of tongue excursion or the mechanics of swallowing, few studies have examined cranial muscle architecture (notable exceptions being Naples, 1999; Smith and Redford, 1990), we do not know if the tongue actually enters the nest to any extent during natural feeding, etc. Now that we know which specific morphological features are convergent we have the opportunity to pin down the adaptive significance of these modifications by examining behavior and function in a comparative context.
Turning to a constraint perspective, we can examine functional, phylogenetic and developmental limitations on structure. Functionally, consider the long and highly extensible tongue formed by the compound sternoglossus muscle. While it is still not clear how ant-eating mammals use their long tongue, we can assume that its extensibility has a biological role. Some movement of the mammalian tongue is due to longitudinal, transverse and circumferential intrinsic muscles that change its shape, so that the tongue operates as a muscular hydrostat (Kier, 1992; Kier and Smith, 1985). Additional movement is caused by extrinsic muscles that arise from various cranial surfaces and enter the base of the tongue, pulling the tongue towards their attachments. Functional constraint arises from the fact that vertebrate muscle is limited in its ability to shorten due to sarcomere structure. A muscle fiber can shorten to approximately 70% of its resting length, so a parallel-fibered muscle has a similar maximum relative shortening. The length of the ant-eating tongue can be viewed as a solution necessitated by this functional constraint: muscular hydrostats that start out long and thin are capable of greater absolute elongation, and the longer extrinsic muscles are capable of greater absolute excursion upon tongue retraction. Through the combination of these features the myrmecophage tongue is capable of being extended farther than the typical eutherian tongue.
On top of these purely functional considerations, we can examine ways in which the ancestral nature of the mammalian feeding apparatus constrains the evolution of structure. I will use the tongue example again. Several of the mammalian extrinsic tongue muscles originate from the hyoid apparatus. Consequently, tongue excursion beyond that provided for by shortening of the muscles themselves is dependent on the mobility of the hyoid. Sloths have an especially mobile hyoid (Naples, 1986) and use their squat tongues to grasp leaves, but there are limits to the extension that can be achieved when the tongue is anchored to the hyoid. An alternative strategy can be seen in anteaters and pangolins: the tongue has lost most of its cranial attachments. One muscle is absent (styloglossus), another has retreated from the body of the tongue (palatoglossus), and a third remains in the tongue but has detached from the hyoid (hyoglossus). Only the genioglossus remains to anchor the tongue to the head. Freeing the tongue from the hyoid removes a limit on tongue excursion imposed by the basic architecture of the mammalian feeding apparatus. Moreover, this modification is what actually enables the extreme lengthening of the tongue (i.e., fusion of the hyoglossus and sternohyoideus to form a sternoglossus). Thus, we can understand the similarities seen in tongue construction in ant-eating mammals as perhaps the only solution to a common functional problem, a need for extreme extensibility, given their shared ancestral pattern of feeding apparatus muscles.
On top of such functional and phylogenetic considerations, we can add the insight provided by consideration of the developmental basis for structural modifications seen in ant-eating mammals. Linking development to convergence depends in part on determining whether shared adult morphology is the result of similar modifications in the developmental program. If this can be demonstrated, then we can ask whether similar ontogenetic changes reflect the existence of a developmental constraint. For example, cranial muscle connective tissues have been shown to arise from the same neural crest populations as do the skeletal elements to which the muscles attach (Köntges and Lumsden, 1996). Returning to the tongue example, we can hypothesize that the formation of a sternoglossus is related to the failure of relevant neural crest cells to populate the developing muscle precursors, thus altering the patterning of their attachments. This mechanism could be ubiquitous in mammals with a sternoglossus, or there could be other processes at work, e.g., some other breakdown in signaling between the developing hyoglossus and sternohyoideus and their usual target skeletal tissue, the hyoid. It would be unreasonable to undertake this developmental work in myrmecophages—it's hard enough to find adults to dissect. However, general questions regarding the developmental basis of variation in hyoid muscle attachments could be pursued in less rare taxa by focusing instead on the compound digastric muscle, which varies widely across all taxonomic levels in its degree of hyoid attachment (Edgeworth, 1914; Evans, 1959; Saban, 1968; Toldt, 1908).
Ontogenetic pathways themselves can operate as a constraint when derived similarities result from truncation of a shared ancestral pathway. Such deletion of later stages in a recapitulated ontogeny might explain similarities seen between the posterior digastric of anteaters and pangolins, and between these two taxa and echidnas. The posterior digastric of anteaters and pangolins has no attachment to either the anterior digastric or the hyoid, but rather, attaches to its antimer across the midline. Edgeworth called this muscle the interhyoideus, noted its presence in monotreme adults, and also noted that many eutherians recapitulate this stage in the ontogeny of the compound digastric muscle (Edgeworth, 1914, 1923, 1935). These observations suggest that the posterior digastric of anteaters and pangolins, which contributes to the unique muscular sheath surrounding the tongue, is a convergent atavism shared due to a common ancestral ontogenetic pathway.
I have used the tongue and posterior digastric as examples to illustrate inquiries concerning constraint, but a similar approach can be applied to palatal and pharyngeal modifications as well. Functional, phylogenetic, and developmental limitations on the evolution of structure do not represent exclusive alternatives in the causes of convergence any more than adaptation and constraint represent exclusive alternatives. Rather, all of these perspectives should, ideally, be parallel lines of inquiry that together provide a rich picture of the many factors that guide morphological evolution.
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SYNOPSISINTRODUCTIONXENARTHRA AND PHOLIDOTAOTHER MAMMALIAN MYRMECOPHAGESEXPLAINING PATTERNS OF...CONCLUSIONSReferences |
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The ability to articulate and test hypotheses regarding causation in morphological evolution is ultimately dependent on our ability to define the patterns of evolutionary change. In the case of the ant-eating mammals, I have combined detailed anatomical investigations with phylogenetic analyses in an attempt to clarify these patterns and formulate more precise questions regarding the causes of convergence. There exist better studied examples of convergence (e.g., the work of Wake and colleagues on plethodontid salamanders, see Wake, 1991
, and references therein). Much work remains to be done on ant-eating mammals, and it will be interesting to see if future character and phylogenetic analyses will bear out the conclusions advanced here. For example, a large proportion of xenarthran and marsupial taxonomic diversity has not been studied anatomically, and this limits our confidence in reconstructions of ancestral character states in both of these groups. Similarly, future phylogenetic analyses may force revision of the relationships (or more appropriately, the lack thereof) among the myrmecophagous mammals discussed here. Nevertheless, a foundation for continuing work now exists. Specific functional hypotheses can be formulated and tested; particular developmental processes can be investigated. The results of these studies are certain to futher clarify the processes responsible for the evolution of strikingly unusual and strikingly similar feeding apparatus morphology in the most specialized myrmecophagous mammals.
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ACKNOWLEDGMENTS |
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Don Swiderski kindly invited me to participate in the symposium from which this manuscript arose. My dissertation work, facilitated by my committee, Deedra McClearn, Amy McCune, and Milo Richmond, the administrative staff of Cornell's Section of Ecology and Systematics, and NSF DEB-9321482, forms the basis for the ideas presented here. Several annonymous reviewers have helped me sharpen my thoughts through successive iterations of this work, and John Reiss continues to provide valuable scientific and editorial criticism.
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FOOTNOTES |
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1 From the Symposium Beyond Reconstruction: Using Phylogenies to Test Hypotheses About Vertebrate Evolution presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 4–8 January 2000, at Atlanta, Georgia.
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