Jörg Habersetzer

Chemical, experimental, and morphological evidence for diagenetically altered melanin in exceptionally preserved fossils

Significance Melanin is a widespread pigment that provides black to reddish brown hues to organisms. Recent evidence has shown that melanin is retained in exceptionally preserved fossils, including feathered dinosaurs, allowing the reconstruction of ancient color patterns. However, little is known about the chemical preservation of melanin or its distribution in the fossil record. Here, we show that melanin is preserved in a number of soft-bodied fossils, but its burial under high pressure and temperature for millions of years alters its original chemistry. The widespread occurrence of melanin substantiates the applicability of reconstructing aspects of original color patterns and allows us to dismiss the alternative suggestion that these structures are microbial in origin. In living organisms, color patterns, behavior, and ecology are closely linked. Thus, detection of fossil pigments may permit inferences about important aspects of ancient animal ecology and evolution. Melanin-bearing melanosomes were suggested to preserve as organic residues in exceptionally preserved fossils, retaining distinct morphology that is associated with aspects of original color patterns. Nevertheless, these oblong and spherical structures have also been identified as fossilized bacteria. To date, chemical studies have not directly considered the effects of diagenesis on melanin preservation, and how this may influence its identification. Here we use time-of-flight secondary ion mass spectrometry to identify and chemically characterize melanin in a diverse sample of previously unstudied extant and fossil taxa, including fossils with notably different diagenetic histories and geologic ages. We document signatures consistent with melanin preservation in fossils ranging from feathers, to mammals, to amphibians. Using principal component analyses, we characterize putative mixtures of eumelanin and phaeomelanin in both fossil and extant samples. Surprisingly, both extant and fossil amphibians generally exhibit melanosomes with a mixed eumelanin/phaeomelanin composition rather than pure eumelanin, as assumed previously. We argue that experimental maturation of modern melanin samples replicates diagenetic chemical alteration of melanin observed in fossils. This refutes the hypothesis that such fossil microbodies could be bacteria, and demonstrates that melanin is widely responsible for the organic soft tissue outlines in vertebrates found at exceptional fossil localities, thus allowing for the reconstruction of certain aspects of original pigment patterns.

Tachypteron franzeni n. gen., n. sp., earliest emballonurid bat from the Middle Eocene of Messel (Mammalia, Chiroptera)

A new genus and species of emballonurid microchiropteran,Tachypteron franzeni, is described from the early Middle Eocene (MP 11) of Grube Messel, near Darmstadt, Germany. The holotype is extraordinarily well-preserved. It is the first unequivocal representative of an extant clade among Messel bats and the oldest unequivocal record of Emballonuridae. The flight apparatus ofT. franzeni is highly specialized for a rapid and constant flight style. The proportions of the strikingly narrow wing, the outline of the flight membranes and external ear, the morphology of the postcranial skeleton, and the relative cochlea size ofT. franzeni and extantTaphozous species are almost identical, while the dentition ofT. franzeni is distinguished by more plesiomorphic features.Tachypteron and the fairly diverse Paleogene record of emballonurids from France, consisting mainly of isolated teeth, document the earliest radiation known from an extant bat family and suggest a rather intense pre-Middle Eocene diversification of emballonurids.KurzfassungEs wird eine neue Gattung und Art der Microchiropteren-Familie Emballonuridae,Tachypteron franzeni, aus dem unteren Mittel-Eozän (MP 11) der Grube Messel bei Darmstadt, Hessen, beschrieben. Der Holotypus ist außergewöhnlich gut erhalten.T. franzeni ist der erste unzweideutige Angehörige einer modernen Familie in der Messeler Fledermausfauna und zugleich der älteste unzweideutige Nachweis der Familie Emballonuridae. Der Flugapparat vonT. franzeni ist extrem spezialisiert für einen schnellen und stetigen Flug. Die Proportionen des auffallend schmalen Flügels, der Umriss der Flughäute und des äußeren Ohrs, die Morphologie des post-kranialen Skeletts sowie die relative Cochlea-Größe vonT. franzeni und rezenten Arten der GattungTaphozous sind nahezu identisch. Dagegen unterscheidet sichT. franzeni durch einige plesiomorphe Gebißmerkmale.T. franzeni und die recht vielgestaltigen Nachweise paläogener Emballonuriden aus Frankreich, meistens Einzelzähne, belegen die früheste von einer rezenten Fledermausfamilie bekannte Radiation und weisen auf ziemlich intensive evolutive Prozesse der Emballonuriden vor dern Mittel-Eozän hin.

Paleoecology of early middle Eocene bats from Messel, FRG. aspects of flight, feeding and echolocation

By their diversified flight apparatus Messel bats occupied specific flight niches similar to those of extant tropical bats. The small Palaeochiropteryx tupaiodon is considered to be most specialized for hunting close to the ground and for hovering inside dense vegetation. Contrarily, Hassianycteris spp. most likely were high and fast flyers in the open space. The analysis of gut contents proves that Palaeochiropteryx spp. exclusively fed on small moths and caddis flies, i.e. slow and low flying insects. For P. tupaiodon this confirms the foraging strategy independently from wing morphology. Hassianycteris spp. preyed mainly on beetles or other insects with thick cuticules. Inner ears of Messel microbats are less specialized compared to those of recent species. Especially P. tupaiodon shows no acoustical specialization with regard to its hunting habitat. Thus, we assume that during the early evolution of bats the development of different flight styles and wing shapes preceded acoustical refinements of the ...

Inferring echolocation in ancient bats.

Arising from: N. Veselka et al. 463, 939–942 (2010)10.1038/nature08737; Veselka et al. replyLaryngeal echolocation, used by most living bats to form images of their surroundings and to detect and capture flying prey, is considered to be a key innovation for the evolutionary success of bats, and palaeontologists have long sought osteological correlates of echolocation that can be used to infer the behaviour of fossil bats. Veselka et al. argued that the most reliable trait indicating echolocation capabilities in bats is an articulation between the stylohyal bone (part of the hyoid apparatus that supports the throat and larynx) and the tympanic bone, which forms the floor of the middle ear. They examined the oldest and most primitive known bat, Onychonycteris finneyi (early Eocene, USA), and argued that it showed evidence of this stylohyal–tympanic articulation, from which they concluded that O. finneyi may have been capable of echolocation. We disagree with their interpretation of key fossil data and instead argue that O. finneyi was probably not an echolocating bat.

Evolutionary History of Bats: Systematics and paleobiogeography of early bats

Introduction The phylogenetic and geographic origins of most extant mammalian orders are still poorly documented. Many first appear in the fossil record during the Paleocene-Eocene Thermal Maximum (PETM) at the beginning of the Eocene epoch about 55.5 million years ago (Smith et al ., 2006). However, three prominent orders are exceptions to this pattern. Rodents first appeared in North America about 0.5–1.0 million years before the PETM, but probably had an Asian origin like other Glires (Meng et al ., 2003). Bats and whales are not known with any certainty before Middle Ypresian, about 54 mya. The earliest known bats are small, insectivorous forms that are preserved in both terrestrial and lacustrine fossil faunas. Their phylogenetic and geographic origins are still unknown, although the absence of clear transitional forms in the fossil record suggests that bat origins are potentially either quite ancient or their evolution from non-volant mammals was quite rapid. Although morphological evidence has generally supported an origin from within Euarchontoglires, sequence data from multiple genes strongly supports an origin of bats from within Laurasiatheria (Springer et al ., 2003; Gunnell and Simmons, 2005). The oldest known fossil bats are early-middle Early Eocene taxa, and the first members of modern bat families and superfamilies seem to appear in the fossil record in the Middle Eocene (Gunnell and Simmons, 2005). We thus here restrict the term “early bats” to the species known from the Early and early-middle Middle Eocene (Ypresian and Lutetian, and global equivalents, encompassing European mammalian reference levels MP7 through MP13). These early bats mainly include “eochiropterans” (Eochiroptera Van Valen 1979 is a controversial paraphyletic group composed of primitive taxa; see Simmons and Geisler, 1998 for an overview) and a few taxa belonging to the first members of modern families.

Palaeopathology and fate of Ida (Darwinius masillae, Primates, Mammalia)

The skeletons of the left and right hands of Ida (Darwinius masillae) were analysed with micro-CT. Evidently, a severe trauma has affected the wrist of the right hand at a time when the carpals were not yet ossified. The background of this accident is discussed.

Description of a Well Preserved Fetus of the European Eocene Equoid Eurohippus messelensis.

The early Middle Eocene locality of Grube Messel, near Darmstadt (Germany), is famous for its complete vertebrate skeletons. The degree of preservation of soft tissues, such as body silhouettes, internal organs and gut contents, is frequently remarkable. The present specimen was analyzed for remnants of the reproductive system. Classic anatomy and osteology and high-resolution micro-x-ray were applied to describe the fetus of the European Eocene equoid Eurohippus messelensis. Scanning electronic microscopy (SEM) was used for determination of soft tissue remnants. The fetus is the earliest and best-preserved fossil specimen of its kind. The postcranial fetal skeleton is almost complete and largely articulated, allowing the conclusion that the pregnant mare was in late gestation. The apparent intrauterine position of the fetus is normal for the phase of pregnancy. Death of mare and fetus were probably not related to problems associated with parturition. Soft tissue interpreted as the uteroplacenta and a broad uterine ligament are preserved due to bacterial activity and allow considerations on the evolutionary development of the structures.

Reply to Sauther and Cuozzo 2012

Referring to long-term studies of living lemurs, Sauther and Cuozzo (2012) advanced doubts concerning our interpretation of a serious injury and its consequences for “Ida” (Darwinius masillae)—the famous fossil primate from the early middle Eocene of Grube Messel (Germany) (Franzen et al. 2011, 2012).We appreciate the intense efforts and the immense value of field studies for the interpretation of the palaeobiology of fossils, but we have objections concerning the comparisons and conclusions of Sauther and Cuozzo (2012).