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Phylogenetic Relationships of Icaronycteris, Archaeonycteris, Hassianycteris, and Palaeochiropteryx to Extant Bat Lineages, With Comments on the Evolution of Echolocation and Foraging Strategies in Microchiroptera

Journal / Magazine

Series: Bulletin of the American Museum of Natural History (AMNH Bulletins) Volume: 235

By: Nancy B Simmons(Author), Jonathon H Geisler(Author)

American Museum of Natural History

Paperback | Dec 1998 | #98389
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NHBS Price: £26.50 $34/€29 approx

About this book

The Eocene fossil record of bats (Chiroptera) includes four genera known from relatively complete skeletons: Icaronycteris, Archaeonycteris, Hassianycteris, and Palaeochiropteryx. Phylogenetic relationships of these taxa to each other and to extant lineages of bats were investigated in a parsimony analysis of 195 morphological characters, 12 rDNA restriction site characters, and one character based on the number of R-1 tandem repeats in the mtDNA d-loop region.

Results indicate that Icaronycteris, Archaeonycteris, Hassianycteris, and Palaeochiropteryx represent 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 both Megachiroptera and Microchiroptera (e.g., Eochiroptera) or a separate 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 features of this classification include restriction of Microchiroptera to the smallest clade that includes all extant bats that use sophisticated echolocation (Emballonuridae + Yinochiroptera + Yangochiroptera), and formal recognition of two more inclusive clades that encompass Microchiroptera plus the four fossil genera. Comparisons of results of separate phylogenetic analyses including and subsequently excluding the fossil taxa indicate that inclusion of the fossils changes the results in 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), and also changes the levels at which transformations appear to apply (hence altering perceived support for some clades).

Results of an additional phylogenetic analysis in which soft-tissue and molecular characters 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 evolution of flight was followed by the origin of low-duty-cycle laryngeal echolocation in early members of the microchiropteran lineage. This system was most likely simple at first, permitting orientation and obstacle detection but not detection or tracking of airborne prey. Owing to the mechanical coupling of ventilation and flight, the energy costs of echolocation to flying bats were relatively low. In contrast, the benefits of aerial insectivory were substantial, and a more sophisticated 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 capture, may have resulted in reduction and simplification of the visual system as echolocation became increasingly important.

Our analysis confirms previous suggestions that Icaronycteris, Archaeonycteris, Hassianycteris, and Palaeochiropteryx used echolocation. Foraging strategies of these forms were reconstructed based on postcranial osteology and wing form, cochlear size, and stomach contents. In the context of our phylogeny, we suggest that foraging behavior in the microchiropteran lineage evolved in a series of steps: (1) gleaning food objects during short flights from a perch using vision for orientation and obstacle detection; prey detection by passive means, including vision and/or listening 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 means (Icaronycteris, Archaeonycteris); (3) perch hunting for both stationary and flying prey using echolocation and vision for 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 times); (4) combined perch hunting and continuous aerial hawking using echolocation and vision for orientation and obstacle detection; prey detection and tracking using echolocation for flying prey and passive means for stationary prey; calcar-supported uropatagium used for prey capture (common ancestor of Hassianycteris and Palaeochiropteryx; retained in Palaeochiropteryx); (5) exclusive reliance on continuous aerial hawking using echolocation and vision for orientation and obstacle detection; prey detection and tracking using echolocation (Hassianycteris; common ancestor of Microchiroptera).

The transition to using echolocation to detect and track prey would have been difficult in cluttered environments owing to interference produced by multiple returning echoes. We therefore propose that this transition occurred in bats that foraged in forest gaps and along the edges of lakes and rivers in situations where potential perch sites were adjacent to relatively clutter-free open spaces. Aerial hawking using echolocation to detect, track, and evaluate prey was apparently the primitive foraging strategy for Microchiroptera. This implies that gleaning, passive prey detection, and perch hunting among extant microchiropterans are secondarily derived specializations rather than retentions of primitive habits. Each of these habits has apparently evolved multiple times. The evolution of continuous aerial hawking may have been the 'key innovation' responsible for the burst of diversification in microchiropteran bats that occurred during the Eocene. Fossils referable to six major extant lineages are known from middle-late Eocene deposits, and reconstruction of ghost lineages leads to the conclusion that at least seven more extant lineages were minimally present by the end of the Eocene.

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