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Family Phyllostomidae Gray 1825 (Chiroptera): summary 2000 to 2018

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The bat family Phyllostomidae has undergone one of the largest known adaptive radiations among mammals; currently it is the second most diverse family of bats after Vespertilionidae and the most diverse with respect to feeding habits. Consequently,
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  Special Publications Museum of Texas Tech University  Number xx xx XXXX 2010 Title     Special Publications Museum of Texas Tech University  Number 71 11 October 2019 From Field to Laboratory: A Memorial Volume In Honor of Robert J. Baker Edited by Robert D. Bradley, Hugh H. Genoways, David J. Schmidly, and Lisa C. Bradley   F AMILY  P HYLLOSTOMIDAE  G RAY  1825 (C HIROPTERA ): S UMMARY  2000 TO  2018  L  IZETTE   S   ILES     AND  R ODRIGO  S. R  IOS  A BSTRACT The bat family Phyllostomidae has undergone one of the largest known adaptive radiations among mammals; currently it is the second most diverse family of bats after Vespertilionidae and the most diverse with respect to feeding habits. Consequently, the Phyllostomidae plays a vital role in ecosystem processes, which include forest regeneration, plant pollination, and insect predation. These characteristics make phyllostomids a fascinating group to study and current research is very dynamic. In this review, a summary of the state of knowledge regard -ing three main aspects of phyllostomids is provided—rapid diversication, systematics, and recent taxonomic changes. First, the rapid diversication in the family is explored, and then the morphological, ecological, historical, and genetic processes that allowed this diversication to occur are discussed. Systematics and taxonomy in Phyllostomidae have been inuenced by the intense molecular work carried out in recent decades. Early results showed that molecular and morphological phylogenies of Phyllostomidae were not congruent and revealed that feed - ing guilds were not necessarily monophyletic. Since then, numerous efforts have been made to resolve the family comprehensively and a discussion of the most recently published phylogenies is included. Taxonomically, new species have been described every year since the last revision in 2005, which resulted in a 34% increase in number of species, accounting for approximately 60% of all bats described in the Neotropics. A detailed review of these changes is presented, which includes described species, elevated subspecies or synonyms, and synonymized species. Taxonomic revisions were focused on only 10 of the 60 phyllostomid genera, thus research opportunities in this area are extensive. Future work promises to be equally intense to obtain an accurate description of the family’s diversity, dene speciation patterns, provide an accurate taxonomy for ecological and behavioral studies, and delimit species distributions. Key words: Chiroptera, Neotropics, Phyllostomidae, rapid diversication, systematics, taxonomy I NTRODUCTION One of biology’s most fundamental and recogniz - able patterns is that species diversity is highest in the tropical regions of the world, with a few exceptions (Willlig et al. 2003). Explanations for this pattern date to Dobzhansky (1950) and competitive arguments have  been circular or contradictory (Lugo 1988). A review  by Mittelbach et al. (2007) summarized three kinds of explanations for the pattern: ecological hypotheses that focus on species coexistence and diversity main - tenance, evolutionary hypotheses that focus on rates of diversication, and historical hypotheses that focus on the duration and extent of tropical environments in Earth’s history. The latitudinal diversity gradient is particularly true for mammals in the New World tropics. Originally dened by Wallace (1876), the Neotropical region includes South America, tropical North America, and the Antilles, and is dened by its large proportion of lowlands, tropical forests, a large mountain range, favorable climate, and a high diversity of genera and species. Currently, more than 1,500 species of mam - mals have been described from this region, which is approximately 30% of all extant mammal species (Patterson and Costa 2012). In the case of Chiroptera, approximately 100 species of bats have been estimated to occur in sympatry (Voss and Emmons 1996), but the highest bat diversity sampled has yielded 78 species in a 3 km radius (Simmons and Voss 1998). A single area can only support this many species through an ef  - fective resource partitioning among competing species (Hutchinson 1959; Giller 1984). 131  132 S PECIAL  P UBLICATIONS , M USEUM   OF  T EXAS  T ECH  U NIVERSITY There are several speciose endemic mammalian groups that occur in the Neotropics, e.g. platyrrhine monkeys, caviomorph rodents, and sigmodontine rodents. However, bats of the family Phyllostomidae are recognized as being the most ecologically diverse  because they comprise species with all the dietary strategies used by Chiroptera (Baker et al. 2012). Bat families that are also endemic to this region, are very  poor in diversity (Furipteridae, Mormoopidae, Na - talidae, Noctilionidae, and Thyropteridae) (Table 1). Other bat families that have a cosmopolitan distribution are less diverse than phyllostomids in the Neotropics: Emballonuridae has 23 species, Molossidae 51, and Vespertilionidae 85 (Solari and Martínez-Arias 2014). Overall, the Phyllostomidae has the largest number of genera and is the second most speciose bat fam - ily after Vespertilionidae (Table 1). It is distributed mostly across the Neotropics, but can also be found in the extreme southwestern United States (Villalobos and Arita 2010).The Phyllostomidae is one of the most highly studied bat families encompassing almost every aspect of its biology. Its high species diversity, adaptations, feeding guilds, and rapid diversication make it a fas- cinating group to study. Perhaps another contributing factor is that its members are the most easily captured species using traditional mist-netting techniques. Dr. Robert J. Baker (1942–2018) was captivated by phyl - lostomid bats from the beginning of his career (Geno - ways et al. 2018) and contributed enormously to our current knowledge of the family. This review focuses on three topics of Dr. Baker’s work and legacy within the group. The rst topic describes the morphological, historical, ecological, and genetic processes that have contributed to the rapid diversication in phyllosomid  bats. The second topic summarizes the recent system - atics of the family, and the third topic details recent taxonomic changes. Table 1. Current taxa within bat families based on information from www.itis.gov, excluding Phyllostomidae, which is based on published records through  November 2018. Bat FamiliesSubfamiliesGeneraSpeciesSubspeciesVespertilionidae550456397Phyllostomidae1160218126Pteropodidae244195205Molossidae216119100Rhinolophidae195144Hipposideridae99489Emballonuridae145361Miniopteridae113134 Nycteridae11618 Natalidae312Mormoopidae21022Rhinopomatidae1610Megadermatidae4522Thyropteridae155Furipteridae22Mystacinidae12Myzopodidae12 Noctilionidae126Cistugidae12Craseonycteridae 11  S ILES   AND  R  IOS  —P HYLLOSTOMIDAE : S UMMARY  2000 TO  2018 133R  APID  D IVERSIFICATION   IN  P HYLLOSTOMID  B ATS It is evident that the family Phyllostomidae has undergone one of the largest known adaptive radiations among mammals (Baker et al. 2003, 2012; Freeman 2000; Dumont et al. 2012). The srcin of Phyllos - tomidae occurred approximately 35 million years ago (MYA) (Baker et al. 2012; Amador et al. 2018), but most species have diversied in a short time period. Of the 154 valid species analyzed by Amador et al. (2018), 58.4% evolved in the last 5 million years and 80.5% in the last 10 million years (58% of all phyllostomids), leaving a small window of evolutionary time for these major adaptive changes to have accumulated (Fig. 1). The possible scenario that allowed this diversication includes eco-morphological, historical and ecological, and genetic processes.  Eco-morphological processes .— The most strik  - ing and perceptible characteristic of the species in Phyl - lostomidae is their morphological adaptations and how these relate to the ecological role they perform in the environment, specically regarding their diet. Based on phylogenetic data and the widespread occurrence of insectivory, it is more parsimonious to assume that this was the feeding strategy of the common ancestor of all members of this family (Freeman 2000; Baker et al. 2012). The primitive insectivore of the Phyl - lostomidae was not very differentiated in morphology from the modern insectivorous species that eat some  plant material and are located at the base of the phylo - genetic tree, i.e.  Macrotus  and  Micronycteris  (Freeman 2000; Baker et al. 2012). These genera have retained ancestral characteristics for teeth, reproductive histo -morphology (Hood and Smith 1982), and post-cranial anatomy (Walton and Walton 1968). It is likely that a minor change in jaw mechanics occurred, which had major implications at the tooth-food interface (Freeman 2000), producing an unusual insectivorous bat that was able to eat at least some plant material (Freeman 2000; Baker et al. 2012). This change in ecology sets the bas - es for further variation in diet and great morphological diversication, allowing phyllostomids to escape the insectivore morphospace into different feeding guilds.In the case of carnivores, changes in tooth mor  -  phology, such as larger teeth relative to the palate and an enlarged protoconid in the lower molars (Freeman 1998) allowed these bats to feed on small vertebrates. This change in diet allowed an increase in the body mass due to the larger prey, therefore escaping the insectivorous morphospace by signicantly increasing its body size (Freeman 2000), e.g. Vampyrum spectrum (171–180 g) and Chrotopterus auritus (62–77 g). How - ever, Santana et al. (2011) discovered that the much smaller  Micronycteris microtis  (7 g) could feed on anole lizards, which not only makes it the smallest carnivore reported to date, but also broadens signicantly their ecological niche and exhibits their plasticity.Bats that shifted their diet from insects to fruit are likely to share this derived character of Phyllostomidae, therefore frugivory may be the dietary pleisiomorphy of the family (Baker et al. 2012). Currently, frugivorous  bats comprise the most speciose feeding guild within the family (3 subfamilies, 107 species). Some frugivo - res retained the ancestral cranial and tooth morphology (e.g., Carollia,  Freeman 2000) and a portion of their diet includes insects, whereas others have evolved teeth specialized for processing only fruit (e.g., Centurio ), which in turn modied greatly the overall skull pattern towards a short rostrum and round braincase. For nectar and pollen-feeding bats, most of the   morphological changes included the lengthening of the rostrum and a size reduction of the teeth (Fig. 2) (Free - man 2000). The specialization of the tongue (elongated and hirsute) to collect nectar is one of the most extreme among mammalian nectivores (Freeman 1998). Simi - larly to Carollia  for the frugivores, some species like Glossophaga soricina  have retained the most ancestral form, whereas other species have evolved extreme morphological modications (Freeman 2000), e.g.  Anoura fstulata  with a tongue that is 150% its body length (Muchhala et al. 2005), and the elongated skulls of  Musonycteris harrisoni  and  Platalina genovensium  (Fig. 2). A third morphological pattern can be observed in the island-dwellers of the tribe Brachyphyllini (Fig. 2), which evolved away from specialized nectarivory to a more frugivorous, orivorous, and generalized diet (Freeman 2000).Only two groups of vertebrates are obligate  blood-feeders, catsh of the subfamily Vandellinae,  134 S PECIAL  P UBLICATIONS , M USEUM   OF  T EXAS  T ECH  U NIVERSITY Figure 1. Dated phylogeny of the family Phyllostomidae (modied from Amador et al. 2018). Black lled circles: posterior probability ≥ 0.95, gray lled circles: posterior probability < 0.95, with high posterior density intervals for node ages. Taxonomic arrangement follows Baker et al. (2016). Geological events are modied from Hoorn et al. (2010). Red triangles and lines: periods of intensied Andean uplift; Panama: closing of Panama Isthmus and start of GABI; Acre: uvial Western Amazonian wetland; Pebas system: large wetland of shallow lakes and swamps in Western Amazonia; GAAR: Greater Antilles-Aves Ridge; and Pozo system: large extension of Amazonia over most of northern South America.
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