PHYLOGENETIC-RELATIONSHIPS OF ICARONYCTERIS, ARCHAEONYCTERIS, HASSIANYCTERIS, AND PALAEOCHIROPTERYX TO EXTANT BAT LINEAGES, WITH COMMENTS ON THE EVOLUTION OF ECHOLOCATION AND FORAGING STRATEGIES IN MICROCHIROPTERA

The Eocene fossil record of bats (Chiroptera) includes four genera kno wn from relatively complete skeletons: Icaronycteris, Archaeonycteris, Hassianycteris, and Palaeochiropteryx. Phylogenetic relationships of these taxa to each other and to extant lineages of bats were investiga ted in a parsimony analysis of 195 morphological characters, 12 rDNA r estriction site characters, and one character based on the number of R -1 tandem repeats in the mtDNA d-loop region. Results indicate that Ic aronycteris, Archaeonycteris, Hassianycteris, and Palaeochiropteryx re present a series of consecutive sister-taxa to extant microchiropteran bats. This conclusion stands in contrast to previous suggestions that these fossil forms represent either a primitive grade ancestral to bo th Megachiroptera and Microchiroptera (e.g., Eochiroptera) or a separa te clade within Microchiroptera (e.g., Palaeochiropterygoidea). A new higher-level classification is proposed to better reflect hypothesized relationships among Eocene fossil bats and extant taxa. Critical feat ures of this classification include restriction of Microchiroptera to the smallest clade that includes all extant bats that use sophisticate d echolocation (Emballonuridae + Yinochiroptera + Yangochiroptera), an d formal recognition of two more inclusive clades that encompass Micro chiroptera plus the four fossil genera. Comparisons of results of sepa rate phylogenetic analyses including and subsequently excluding the fo ssil taxa indicate that inclusion of the fossils changes the results i n two ways: (1) altering perceived relationships among extant forms at a few poorly supported nodes; and (2) reducing perceived support for some nodes near the base of the tree. inclusion of the fossils affects some character polarities (hence slightly changing tree topology), an d also changes the levels at which transformations appear to apply (he nce altering perceived support for some clades). Results of an additio nal phylogenetic analysis in which soft-tissue and molecular character s were excluded from consideration indicate that these characters are critical for determination of relationships among extant lineages. Our phylogeny provides a basis for evaluating previous hypotheses on the evolution of flight, echolocation, and foraging strategies. We propose that flight evolved before echolocation, and that the first bats used vision for orientation in their arboreal/aerial environment. The evol ution of flight was followed by the origin of low-duty-cycle laryngeal echolocation in early members of the microchiropteran lineage. This s ystem was most likely simple at first, permitting orientation and obst acle detection but not detection or tracking of airborne prey. Owing t o the mechanical coupling of ventilation and flight, the energy costs of echolocation to flying bats were relatively low. In contrast, the b enefits of aerial insectivory were substantial, and a more sophisticat ed low-duty-cycle echolocation system capable of detecting, tracking, and assessing airborne prey subsequently evolved rapidly. The need for an increasingly derived auditory system, together with limits on body size imposed by the mechanics of flight, echolocation, and prey captu re, may have resulted in reduction and simplification of the visual sy stem as echolocation became increasingly important. Our analysis confi rms previous suggestions that Icaronycteris, Archaeonycteris, Hassiany cteris, and Palaeochiropteryx used echolocation. Foraging strategies o f these forms were reconstructed based on postcranial osteology and wi ng form, cochlear size, and stomach contents. In the context of our ph ylogeny, we suggest that foraging behavior in the microchiropteran lin eage evolved in a series of steps: (1) gleaning food objects during sh ort flights from a perch using vision for orientation and obstacle det ection; prey detection by passive means, including vision and/or liste ning for prey-generated sounds (no known examples in fossil record); ( 2) gleaning stationary prey from a perch using echolocation and vision for orientation and obstacle detection; prey detection by passive mea ns (Icaronycteris, Archaeonycteris); (3) perch hunting for both statio nary and Eying prey using echolocation and vision far orientation and obstacle detection; prey detection and tracking using echolocation for flying prey and passive means for stationary prey (no known example, although Icaronycteris and/or Archaeonycteris may have done this at ti mes); (4) combined perch hunting and continuous aerial hawking using e cholocation and vision for orientation and obstacle detection; prey de tection and tracking using echolocation for flying prey and passive me ans for stationary prey; calcar-supported uropatagium used for prey ca pture (common ancestor of Hassianycteris and Palaeochiropteryx; retain ed in Palaeochiropteryx); (5) exclusive reliance on continuous aerial hawking using echolocation and vision for orientation and obstacle det ection; prey detection and tracking using echolocation (Hassianycteris ; common ancestor of Microchiroptera). The transition to using echoloc ation to detect and track prey would have been difficult in cluttered envionments owing to interference produced by multiple returning echoe s. We therefore propose that this transition occurred in bats that for aged in forest gaps and along the edges of lakes and rivers in situati ons where potential perch sites were adjacent to relatively clutter-fr ee open spaces. Aerial hawking using echolocation to detect, track, an d evalute prey was apparently the primitive foraging strategy for Micr ochiroptera. This implies that gleaning, passive prey detection, and p erch hunting among extant microchiropterans are secondarily derived sp ecializations rather than retentions of primitive habits. Each of thes e habits has apparently evolved multiple times. The evolution of conti nuous aerial hawking may have been the ''key innovation'' responsible for the burst of diversification in microchiropteran bats that occurre d during the Eocene. Fossils referable to six major extant lineages ar e known from Middle-Late Eocene deposits, and reconstruction of ghost lineages leads to the conclusion that at least seven more extant linea ges were minimally present by the end of the Eocene.