The Octodontidae Revisited
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THE OCTODONTIDAE REVISITED UNA REVISION DE OCTODONTIDAE Milton Gallardo, R. Ojeda, C. González, and C. Ríos ABSTRACT The monophyletic and depauperate assemblage of South American octodontid rodents has experienced an extensive adaptive radiation from above-ground dwellers to subterranean, saxicolous, and gerbil-like deserticolous life forms. Complex and saltational chromosomal repatterning is a hallmark of octodontid evolution. Recent molecular evidence links these chromosome dynamics with quantum genome size shifts, and probably with reticulate evolution via introgressive hybridization in the desert dwellers Tympanoctomys barrerae and Pipanacoctomys aureus. Genome duplication represents a novel mechanism of evolution in mammals and its adaptive role is reflected in the ability of deserticolous species to colonize the extreme environment of salt flats. Unique to Tympanoctomys is a the rigid bundle of hairs behind the upper incisors which is crucial to efficiently peel saltbush leaves and probably explains its broader distribution relative to P. aureus. This feature, in association with other attributes (e. g., specialized kidneys, large bullae, feeding behavior) has enabled Tympanoctomys to cope with extreme environmental conditions. Key words: Octodontidae, Octodontids, South American mammals, tetraploidy, Tympanoctomys barrerae. RESUMEN Los octodóntidos son un grupo de roedores monofiléticos que han experimentado una extensa radiación adaptativa desde especies que viven en la superficie a formas de vida subterráneas o de tipo gerbos, especializados a la vida desertícola. La evolución de los octodóntidos está marcada por reordenamientos cromsómicos complejos y de tipo saltatorio. Las evidencias moleculares recientes indican una estrecha asociación entre esta dinámica cromosómica, los cambios genómicos cuánticos y la evolución Pp. xx-xx in Kelt, D. A., E. P. Lessa, J. Salazar-Bravo, and J. L. Patton (eds.). xxxx. The quintessential naturalist: honoring the life and legacy of Oliver P. Pearson. University of California Publications in Zoology xx:xx-xx. University of California Publications in Zoology reticulada mediante hibridización introgresiva de los desertícolas Tympanoctomys barrerae y Pipanacoctomys aureus. La duplicación genómica representa un nuevo mecanismo de evolución en los mamíferos y su rol adaptativo se refleja en la habilidad de estas formas desertícolas para colonizar los ambientes extremos de los salares. Un rasgo único de Tympanoctomys son sus cerdas bucales, ubicadas detrás de los incisivos. Esta adaptación es crucial para pelar las hojas de las plantas halofíticas y seguramente constituye la ventaja que explica su mayor distribución en relación a Pipanacoctomys aureus. Este rasgo, asociado a otros atributos ( e.g. riñones especializados, grandes bullas y comportamiento de alimentación) ha permitido la adaptación de Tympanoctomys a estos ambientes de condiciones extremas. Palabras claves: Octodontidae, Octodontids, mamíferos Sudamericanos, tetraploidía, Tympanoctomys barrerae. INTRODUCTION Endemic of South America, octodontid rodents represent a monophyletic, species- poor but ecologically diverse assemblage of genera including above-surface dwellers, deserticolous, fossorial, and strictly subterranean forms (Table 1). Electrophoretic patterns (Köhler et al., 2000), DNA-DNA hybridization data (Gallardo and Kirsch, 2001), and sequencing of nuclear and mitochondrial markers support a basal clade containing the desert specialists, distributed along the eastern slope of the Andes. This clade is genetically distinct from the species distributed along the western slope (Honeycutt et al., 2003). Extensive chromosomal repatterning, absence of intra- or interpopulational chromosome polymorphism and a bidirectional trend of karyotypic evolution are characteristic of the Octodontidae (Gallardo, 1992, 1997). Indeed, a decrease from the modal 2n = 56-58 characterizes Octodontomys gliroides (2n = 38) whereas a saltational increase in diploid number (2n = 102) associated to genome size duplication has been reported for the red vizcacha rat, Tympanoctomys barrerae (Gallardo et al., 2003, 2004a). The recent description of the salt flat dwellers,Pipanacoctomys aureus and Salinoctomys loschalchalerosorum has increased the recognized diversity of the deserticolous octodontids (Mares et al., 2000). The phylogenetic relationships of P. aureus to T. barrerae, its fully biarmed, 92-chromosome karyotype, and its unexpected double genome size provides evidence to advance a hybrid origin for T. barrerae (Gallardo et al., 2004a). Quantum increases of DNA content in the Octodontidae represent a unique trajectory in the group´s diversification and a novel mechanism of genome evolution in mammals. The buccal structures that allowed T. barrerae to feed on halophytic plants, and hence to colonize the arid salt flat formations, reflect the adaptive nature of this novelty. Data at hand have helped our understanding of the groups reticulate history and a shift from the idea that extant octodontids are remnants of a past and wider adaptive radiation (Reig, 1981). All these features make the octodontids a very distinctive group for studying its genome dynamics, and for contrasting macroecological and phylogenetic hypotheses. Here, updated data on the distribution, systematics, and natural history of the Octodontidae are provided, and a model to account for the genome duplication involving T. barrerae and P. aureus is advanced. Table 1.- Ecological diversification of living octodontids and their latitudinal distribution ranges. Sources: Contreras et al., 1987; Mares and Ojeda, 1982; Mares et al., 2000; Nowak, 1991, 1999; Ojeda et al., 1996; Muñoz-Pedreros, 2000; Oyarce et al., 2003; Redford and Eisenberg, 1992. Body Distribution SPECIES Mass (g) Ecoregion Habits Habitat Diet (Latitudinal Range) Gallardo etal.:TheOctodontidaeRevisited Aconaemys fuscus 123 - 134 Andean Semifossorial, Nothofagus and Seeds and bulbs 35° - 36° S –Patagonian colonial Araucaria forests; forest burrows sandy and xerophytic shrubs Aconaemys sagei 83 - 110 Mediterranean, Semifossorial Bunchgrass and ? 37° - 39° S Matorral Nothofagus forests Aconaemys porteri 80-110 Andean forest Semifossorial Nothofagus and Araucaria seeds, 39° - 40º S Araucaria forests bamboo shots Spalacopus cyanus 60 - 110 Andean and Fossorial, Semidesert sandy Geophytes, 27°- 36° S coastal areas colonial loam, pasture Hemicryptophytes burrows lands, Octodon degus 170-260 Mediterranean, Terrestrial, Coastal and central Chenopods, 28°- 33° S Matorral colonial scrublands grasses, forbs, roots, seeds, leaves Octodon bridgesi 155-240 Mediterranean, Scansorial Rocky and dense Leaves, seeds, 34° - 38° S Matorral scrubland grasses Octodon lunatus 130-235 Mediterranean, Scansorial Rocky and dense Shrubs, forbs, 30º - 36° S Matorral coastal scrublands grasses Octodon pacificus 290 Insular habitats Scansorial Mocha Island ? 38° S 3 4 Table 1 (continued). Octodontomys 115 - 176 Highland; Scansorial, Rocky slopes; near Cacti, acacia pods, 15° - 28° S gliroides Puna and superficial rocky walls (pircas) seeds Prepuna burrows, solitary? University ofCaliforniaPublicationsinZoology Octomys mimax 80-110 Lowland ; Saxicollous, Rock outcrops mesquite, shrubs, 28° - 32° S Monte desert, solitary? cacti Tympanoctomys 81 - 104 Lowland; Ground Salt basins; sand chenopodes, 29°- 39ª S barrerae Monte desert; dwellers, dunes mesquite leaves Monte-Chaco burrow ecotone; Monte system, –Patagonia solitary ecotone Pipanacoctomys 107 Monte desert Ground Salt basin chenopodes, 27° S aureus dwellers, mesquite burrow system, solitary Salinoctomys ? Monte-Chaco Ground Salt basin Chenopodes? 30° S loschalchalerosorum ecotone dwellers, burrow system, solitary Gallardo et al.: The Octodontidae Revisited 5 BIOGEOGRAPHY, DISTRIBUTION, AND NATURAL HISTORY The history and evolution of the South American caviomorph rodents has been thoroughly discussed by different authors (Patterson and Pascual, 1972; Reig, 1981; Woods, 1982; and references therein). The most ancestral caviomorph fossil, Platypittamys, known from the Oligocene of Bolivia and Patagonia (Wood and Patterson, 1959; Patterson and Pascual, 1972; Patterson and Wood, 1982) was a generalized ground- dweller lacking the hypsodont teeth that evolved concomitantly as aridity increased (Webb, 1978). The radiation of the octodontids is connected with the Andean orogenesis as exemplified by the major Miocene-Pliocene faunistic diversification and subsequent climatic and vegetational changes (Contreras et al., 1987 and references therein). As the Andes rose up, new wind patterns resulted in different precipitation regimes across the mountain range (Solbrig, 1976; Mares, 1985). While humid forests and scrublands flourished along the western slope of the Andes, a gradual increase in arid conditions took place on its eastern side (Contreras et al., 1987). Central Argentina was already semiarid during the Eocene whereas Patagonia had a humid climate that supported woodlands during early Miocene (Wolkheimer, 1971). The shift to aridity occurred at the Miocene-Pliocene boundary whereas the northern Puna Desert developed as the Andes uplift took place during the Pleistocene (Simpson, 1975). Several families of caviomorph rodents (abrocomids, caviids, chinchillids, and octodontids) evolved to exploit diverse niches in response to the increasing aridity derived from these orogenic events (Mares and Ojeda, 1982; Mares, 1985). The narrow, longitudinal distribution of the Octodontidae ranges from