On the Roles of Phylogeny and Stochasticity in The
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ON THE ROLES OF PHYLOGENY AND STOCHASTICITY IN THE EVOLUTION OF PERENNIBRANCHIATE TROGLOBITIC SALAMANDERS THOMAS R. JONES' Museum of Zoology, University of Michigan, Ann Arbor, MI 48109 USA; 313-936-0134; Bitnet USERGFTV@UMICHUM; Internet [email protected] and D. BRUCE THOMPSON Department of Zoology, Arizona State University, Tempe, AZ 85287 USA 602-263-1556 Key Words: salamander, troglobitic, paedomorphosis, adaptation, speciation, perennibranchiate Suggested running head: Troglobitic salamander evolution 1 Manuscript corresponding author 1 ABSTRACT Many troglobitic salamanders exhibit paedomorphic morphologies including perennibranchiation, a morphology that has been viewed as a specific adaptation to cave environments. We present a reexamination of that assumption in a phylogenetic context. We suggest that the perennibranchiate condition in troglobitic salamanders is not an adaptation to cave life that has evolved repeatedly and independently, but rather is a consequence of historical, i.e., phylogenetic, processes. Perennibranchiation appears to be a synapomorphy of the clade of hemidactyliine salamanders exclusive of Hemidactylium, and as such has not evolved independently in the obligately troglobitic forms. Further, all known proteid salamanders are perennibranchiate, and therefore that morphology cannot be a specific adaptation in Proteus anquinus. We submit that perennibranchiation in troglobitic salamanders is a result of stochastic "entrapment" of epigean species that were polymorphic (or fixed) for a perennibranchiate condition. Cave-dwelling, perennibranchiate Ambystoma tiqrinum mavortium in south-central New Mexico are an example of a possible intermediate stage in the evolution of obligately troglobitic salamanders. Finally, if a genetic propensity for a perennibranchiate polymorphism exists within a lineage, ecological isolation in caves might be a sufficient condition for further morphological divergence and speciation within that lineage. 2 Recently, there has been a renewed awareness of the important union of ecological and adaptive inference with phylogenetic systematics. While much of the discussion has been necessarily methodological (Brooks, 1985; Coddington, 1988; Brooks and McLennan, 1991), few empirical studies have been directed at particular groups of organisms (e.g., Dunham and Miles, 1985; McLennan et al., 1988; Pearson et al., 1988; Donoghue, 1989; Mooi et al., 1989). This body of work correctly suggests that many commonly held assumptions about adaptation and character evolution should be reexamined in a historical context. Herein we present a case study of the evolution of a perennibranchiate morphology in troglobitic salamanders in such a context. A variety of paedomorphic features may comprise the morphology of troglobitic salamanders (see Wake, 1966), the most notable of which are represented in non-metamorphosing, branchiate adults'. The evolution of perennibranchiate troglobitic salamanders often is discussed implicitly as a deterministic process in which metamorphosing, epigean (surface-dwelling) salamander ancestors enter caves, and descendants subsequently evolve a suite of morphological characteristics, including a perennibranchiate condition, that provide them with a selective advantage in the cave environment. Alternatively, we suggest that a perennibranchiate condition in troglobitic salamanders is a consequence of historical, i.e., phylogenetic, processes rather than an adaptation to cave life, and that the commonness of a perennibranchiate condition in troglobitic salamanders is a result of stochastic "entrapment" of epigean species that are already polymorphic (or fixed) for a perennibranchiate condition. We also provide an example of perennibranchiate, cave-dwelling tiger salamanders (Ambvstoma tiqrinum mavortium), that could represent an intermediate stage in the evolution of obligately troglobitic salamanders. We frame our remarks with respect to 1 In the absence of definitive data describing the developmental evolution of a paedomorphic, perennibranchiate morphology, i.e., neoteny or progenesis (sensu Gould, 1977; Alberch et al., 1979), and to facilitate discussion, we use "perennibranchiate" or "mature branchiate" to refer specifically to sexually mature, permanently gilled salamanders ("perennibranchiation" describes the condition), whether that morphology is considered facultative or obligate. 3 West-Eberhard's (1986, 1989) reviews of the evolutionary significance of alternative phenotypes, and close with a comment regarding general attempts to understand the evolution of perennibranchiate salamanders. TROGLOBITIC TAXA AND HYPOTHESES EXPLAINING PERENNIBRANCHIATE MORPHOLOGY There are six genera of true troglobitic salamanders in two families (Brandon, 1971; see Barr and Holsinger, 1985; Holsinger, 1988 for reviews and definitions) (Table 1.). The tribe Hemidactyliini, family Plethodontidae, includes about ten troglobitic species all North American endemics (taxonomy of some groups is unclear, and is likely to change in the near future; P.T. Chippindale and D.M. Hillis, pers. comm.), while the European proteid, Proteus anquinus, is the only form known elsewhere (Brandon, 1971; Sweet, 1984; Barr and Holsinger, 1985). In North America troglobitic salamanders are found in the Valley and Ridge, adjacent Appalachian Plateau, and Dougherty Plain physiographic provinces (in the southeastern USA), the Ozark Mountains of Arkansas, Missouri, Oklahoma and Kansas, and the Edwards Plateau region, Texas. Perhaps the most obvious feature of troglobitic salamanders is that nearly all species are perennibranchiate; only Gyrinophilus subterraneus and Typhlotriton spelaeus metamorphose. Hypotheses explaining evolution of troglobitic organisms fall generally into two catagories, in which epigean forms either 1) actively enter subterranean systems, either to escape harsh surface environments or to exploit unoccupied niches, or 2) enter caves passively as a result of physical forces beyond their control (see Culver, 1982). Hypotheses in the former category emphasizing escape have been advanced for most troglobitic salamanders (Wake, 1966; Brandon, 1971; Duellman and Trueb, 1986) and terrestrial invertebrates (summaries in Culver, 1982; Holsinger, 1988; Holsinger and Culver, 1988). Mitchell and Smith (1972) extended this theme, suggesting that cave colonizers survived inhospitable climates that removed their epigean relatives. Howarth's (1973, 1981) adaptive-shift theory 4 suggests terrestrial invertebrates actively enter new, ecologically "empty" caves (e.g., lava tubes). In the second category, Sweet (1982, 1984) suggested failure of springs following erosion of their water-bearing strata led to underground retreat of epigean, spring-dwelling salamanders along the edge of the Edwards Plateau, Texas. Similar explanations include entry into caves via springs or stream capture, especially in the case of aquatic invertebrates (Holsinger, 1988; Holsinger and Culver, 1988). A perennibranchiate condition in cave salamanders is framed typically as an adaptive response to cave conditions, although hypothesized selective pressures may vary. For example, Hecht and Edwards (1976:669) said, "Proteus, Typhlomolge, Haideotriton, and other troglobitic salamanders resemble each other in many morphological characters as a result of the severe orthoselective pressures of the cave environment. These resemblances are without question the result of convergent evolution." Here we summarize various hypotheses offered to explain the evolution of perennibranchiates, explicitly in troglobitic salamanders. Wake (1966:82) postulated that within caves, perennibranchiate plethodontids might have had a selective advantage over transforming individuals resulting in eventual fixation of the larval morphology. Dent (1968:303) suggested that selective pressures such as food abundance (in aquatic vs. terrestrial cave environments) likely "brought about the rise of neoteny [sic] in caves." Brandon (1971) also suggested a perennibranchiate morphology was a likely evolutionary response to food requirements and availability, in which morphological features of perennibranchs (e.g., neuromasts, spatulate snouts) allow more efficient feeding in permanently dark, aquatic habitats; this idea also has been emphasized by Culver (1982). In addition, perennibranchs avoid energy expenditures necessary for metamorphosis, which might be important in caves where food is less abundant relative to surface habitats (Brandon, 1971). According to Wilbur and Collins (1973), within caves a selective disadvantage may exist for metamorphosing salamanders that leave stable and relatively productive aquatic habitats to enter unproductive terrestrial environments. 5 Bruce (1976) provided life history data on Eurycea neotenes (as currently recognized, an epigean and troglobitic species) suggesting perennibranchiation evolved through lowering size and age at maturity in response to high juvenile mortality and environmentally determined minimum metamorphic size. Although Bruce (1976) did not implicate cave conditions, Sweet (1977:374) argued against Bruce's suggestions, saying perennibranchiate E. neotenes apparently evolved as a response to "selective disadvantages of metamorphosis" in subsurface aquatic habitats where branchiate animals could feed more effectively. Bruce (1979:1000) later modified and extended Brandon's (1971) ideas regarding perennibranchiate Gyrinophilus palleucus, suggesting the prey resource base was the "relevant environmental