The Old World Leaf-nosed Bats, family Hipposideridae, currently include seven genera and 90 species of insectivorous Bats distributed over much of the Palaeotropics. Both the taxonomic and phylogenetic histories of this family are confused. Throughout much of its history, Hipposideridae was considered either a subfamily of the Rhinolophidae (the Horseshoe Bats) or as its sister family within the Rhinolophoidea. Recently, however, the 'Trident Bats' (Cloeotis, Paratriaenops, Rhinonicteris, and Triaenops) were shown to comprise a family-ranked group, the Rhinonycteridae, which is separate from and sister to the Hipposideridae. Even the genus Hipposideros, as it was traditionally understood, appears paraphyletic with respect to the allied genera Asellia, Aselliscus, Coelops, and Anthops. Re-validation of Macronycteris and Doryrhina for groups of Afrotropical endemic species more closely related to each other than to African and Asian members of Hipposideros sensu stricto resolved a number of those issues.
The species richness of Doryrhina, Macronycteris, and Hipposideros differs widely. Most authors recognise two species of Doryrhina (Doryrhina cyclops and Doryrhina camerunensis), five species of Macronycteris (Macronycteris commersoni, Macronycteris cryptovalorona, Macronycteris gigas, Macronycteris thomensis, and Macronycteris vittata), and 83 species of Hipposideros, 10 of which occur in Africa. These are Hipposideros beatus, Hipposideros caffer, Hipposideros curtus, Hipposideros fuliginosus, Hipposideros lamottei, Hipposideros ruber, and Hipposideros tephrus in the bicolor group of Hipposideros; Hipposideros jonesi and Hipposideros marisae in the speoris group, and Hipposideros megalotis in the megalotis group. In addition, three extinct species of Hipposiderid are known from the region: Macronycteris besaoka, from Madagascar, Hipposideros amenhotepos, from Egypt, and Hipposideros kaumbului, from Ethiopia.
As suggested by their checkered taxonomic history, phylogenetic understanding of the Hipposideridae has slowly come into focus. Doryrhina and Macronycteris are two of a dozen generic-group names that were synonymized with Hipposideros for all of the 20th century. Instead of subgenera, taxonomists used the species groups based on morphology. Assessment of Rhinolophoid relationships using an intron supermatrix based on morphology confirmed the early divergence of Hipposiderids and Rhinolophids (estimated at 41 million years ago), thereby substantiating their rank as a separate families. Despite earlier suppositions that the area of origin for Hipposideridae was in Asia or Australia. Recent studies have clearly demonstrated the ancestry of the family (and superfamily) was in Africa. A recent supermatrix analysis with the most comprehensive taxonomic sampling (42 species) confirmed the early divergence of Hipposiderids and Rhinolophids at 41.3 million years ago, but this analysis questioned the validity of both Doryrhina and Macronycteris. This study attributed the paraphyly of Hipposideros sensu lato to limited taxonomic sampling, and also challenged the integrity of the commersoni, cyclops, speoris, and bicolor species groups, arguing that all African species save for Hipposideros jonesi belonged in a single, exclusively African species group.
Although new species of Hipposiderids are regularly discovered and described in Asia, the pace of discovery has been much slower in Africa. Only one extant species has been described since the recognition of Hipposideros lamottei in 1985, and that one, Hipposideros cryptovalorona, was from Madagascar. Surveys of mitochondrial sequences from African Hipposiderids have strongly suggested that supposedly widespread species such as Hipposideros caffer and Hipposideros ruber actually represent complexes of cryptic species. Phylogenetic analyses show that these named species complexes are not monophyletic, resolving clades comprised of Bats identified as both Hipposideros caffer and Hipposideros ruber. These studies have characterised the clades in both morphological and genetic terms, even establishing them in sympatry. However, the uncertain relationship of the identified clades to the many names already proposed for Afrotropical Hipposiderids, many based on incomplete or formalin-preserved specimens, has precluded formally naming them. Incomplete geographic sampling and the lack of evidence from nuclear genes for these populations has also clouded interpretations of this mitochondrial diversity.
In a paper published in the journal ZooKeys on 22 April 2020, Bruce Patterson of the Negaunee Integrative Research Center at the Field Museum of Natural History, Paul Webala of the Department of Forestry and Wildlife Management at Maasai Mara University, Tyrone Lavery, again of the Negaunee Integrative Research Center at the Field Museum of Natural History, and the Threatened Species Recovery Hub at the Australian National University, Bernard Agwanda of the Mammalogy Section at the National Museums of Kenya, Steven Goodman, again of the Negaunee Integrative Research Center at the Field Museum of Natural History, and of the Association Vahatra, Julian Kerbis Peterhans, again of the Negaunee Integrative Research Center at the Field Museum of Natural History, and of the College of Arts and Sciences at Roosevelt University, and Terrence Demos, once again of the Negaunee Integrative Research Center at the Field Museum of Natural History, present the results of a study which used field surveys in Eastern Africa and adjoining regions to offer a new basis for considering the taxonomy and phylogenetics of Afrotropical Hipposiderids.
Patterson et al. sought to answer these questions: (1) Is there compelling evidence to support the recognition of Doryrhina and Macronycteris as distinct Afrotropical genera alongside the Palaeotropical Hipposideros? (2) Which species belong to these groups? (3) Are the traditional species groups of African Hipposiderids monophyletic? Using both mitochondrial and nuclear intron sequences, Patterson et al. also evaluate the question of cryptic species among African Hipposiderids and the possibility of mitochondrial-nuclear discordance.
In terms of cyt-b sequence divergence, clades within Doryrhina are separated by 3.0–5.7% genetic distances, whereas less than 3% separates the four recognised species of Macronycteris. Between Afrotropical Hipposideros, the greatest distances separate Hipposideros jonesi from other lineages (13.4–16.1%). The various numbered clades allied to Hipposideros caffer differ from one another in cyt-b sequences by 2.5–10.3% and clades allied to Hipposideros ruber differ by 3.0–8.2%.
The three Afrotropical Hipposiderid genera differ substantially in terms of their internal genetic differentiation. Clades of Hipposideros are separated by cyt-b p-distances averaging 9.7% (2.5–16.1%), whereas Doryrhina clades average p-distances of 4.8% (3.0–5.7%) and Macronycteris clades 2.7% (2.6–2.9%). Distance values for these genera tend to fall at the lower end of values obtained with similar sampling intensity for species-ranked clades in other Afrotropical Bat genera: 2.5% for Otomops, 9.3% for Miniopterus, 10% for Scotophilus and Rhinolophus, 13.5% for Myotis, and 17% for Nycteris. Fewer cyt-b substitutions on average for these Hipposiderids does not limit support for individual clades, and because distances do not approach those characteristic of substitutional saturation, the cyt-b tree recovers much of the deeper phylogenetic structure evident with nuclear intron sequences.
Both cyt-b and intron analyses securely recovered Doryrhina, Macronycteris, and Hipposideros as monophyletic. Doryrhina + Macronycteris are sister to the remaining Hipposiderids. However, only the cyt-b analysis included the Hipposiderid genera Aselliscus, Coelops, and Asellia alongside Hipposideros. That analysis recovered all four genera as monophyletic with strong support. Aselliscus and Coelops were recovered as sister to Hipposideros, with Asellia joining later, but these relationships lacked confident support.
Using a supermatrix approach on exemplars of 46 species of hipposiderids, a previous study led by Lucila Inés Amador found Hipposideros sensu stricto to be paraphyletic. They recovered a mostly Asian group of Hipposideros as sister to two subclades, Coelops + Aselliscus and Asellia + African Hipposiderids excluding Hipposideros jonesi, which was recovered with the Asian taxa. Paraphyly in this molecular analysis echoed earlier indications of Hipposideros paraphyly from morphology. In another supermatrix analysis of exemplars belonging to 49 hipposiderid species, Jeff Shi and Daniel Rabosky failed to recover Macronycteris as monophyletic; Macronycteris commersoni was sister to all remaining Hipposiderids, but strangely it did not group with Macronycteris gigas. When the anomalous position of Macronycteris commersoni in their tree is ignored, their topology is highly similar to that of Patterson et al., except that Asellia (Aselliscus, Coelops) become the sister of Hipposideros (Macronycteris, Doryrhina), rather than sister of just Hipposideros. Using both mitochondrial and nuclear loci, a previous study by Tyrone Lavery, Luke Leung, and Jennifer Seddon found that 17 species of Asian, Oceanian and Australasian Hipposideros were monophyletic with respect to the genera Aselliscus, Coelops, and Anthops. Clearly, missing data and missing taxa compromise all of these phylogenetic appraisals, so that the question of Hipposiderid and Hipposideros monophyly remains open. However, subject to its sampling limitations, there is clear support in Patterson et al.'s analyses of monophyly for Doryrhina, Macronycteris, and Hipposideros as they apply these names.
Despite employing different mitochondrial and nuclear loci and using different sets of taxa, the phylogeny recovered by Lavery, Leung and Seddon is largely congruent with that of Patterson et al. Their earliest diverging species group of Hipposideros is the calcaratus group, not represented in Patterson et al.'s tree unless Hipposideros obscurus is a member. Lavery et al.'s next diverging unit is the diadema group, which is also positioned near the base of Patterson et al.'s tree. Lavery et al.'s other two groups are paired: the galeritus group (which includes Hipposideros cervinus, indicating that this species is misclassified as a calcaratus member) joined with the bicolor/ater group. In Patterson et al.'s intron analysis, members of the larvatus and diadema groups join Hipposideros obscurus as sister to all remaining Hipposideros groups. The remainder form a trichotomy: Hipposideros coronatus, typically considered in the bicolor group; Hipposideros pygmaeus and Hipposideros cervinus, which are listed in different groups but were both considered members of the galeritus unit by George Tate; and the erstwhile bicolor group, which was subdivided into the ater subgroup (for Asian, Oceanian, and Australasian species) and the ruber subgroup (for Atrotropical ones) by Ara Monadjem.
The ater subgroup members included in Patterson et al.'s mitochondrial analysis form a well-supported clade consisting of Hipposideros bicolor, Hipposideros cineraceus, Hipposideros pomona, Hipposideros doriae, Hipposideros ater, Hipposideros khaokhouayensis, Hipposideros rotalis, Hipposideros halophyllus, Hipposideros dyacorum, Hipposideros ridley, and Hipposideros durgadasi. This group is sister to all analyzed members of the ruber subgroup: the various clades allied with Hipposideros beatus, Hipposideros caffer, and Hipposideros ruber, as well as individuals of the Afrotropical species Hipposideros lamottei and Hipposideros fuliginosus. Hipposideros abae, which was previously considered in the speoris group, is clearly a member of the ruber group. Outside this pairing are the Asian species Hipposideros cervinus, Hipposideros coronatus, Hipposideros coxi, Hipposideros obscurus, and Hipposideros pygmaeus. Two Afrotropical species also lie outside the ruber + ater clade: Hipposideros jonesi and Hipposideros marisae, both thought to belong to the speoris group.
Parsimony, topological position, and the strong support of branching relationships in the mitochondrial and intron trees make it clear that the Afrotropical ruber group represents a comparatively recent colonisation event from Asian ancestors–the ruber group is sister to the ater group and this pair has Asian sisters. However, although the basal dichotomy within Hipposideros includes an all Asian clade, lack of support for its sister(s) clouds the phylogenetic position of the Hipposideros jonesi-Hipposideros marisae clade–possibly sister to all sampled Hipposideros but more likely sandwiched between Asian clades. In any case, Patterson et al.'s analysis suggests that the Hipposideros jonesi-Hipposideros marisae clade resulted from an earlier African-Asian colonisation event.
The lack of agreement in the phylogenetic position of Hipposideros diadema and Hipposideros larvatus between the concatenated intron tree and the species tree deserves comment, as both analyses were based on the same genetic dataset. The position of Hipposideros diadema-Hipposideros larvatus as sister to the ruber group runs counter to both our other genetic analyses and morphological assessments. This discrepancy is likely due to the generally weaker support for deep nodes within the tree; in the absence of saturation, this is often taken as evidence of rapid evolutionary radiations. Hayley Lanier and Lacey Knowles used simulated data on deep phylogenies to show that species-tree methods do account for coalescent variance at deep nodes but that mutational variance among lineages poses the primary challenge for accurate reconstruction. In either case, vastly expanded genetic sampling via NGS techniques offers the most plausible avenues to clearer resolution.
However, the highly distinctive species Hipposideros megalotis belongs to its own species group and has not been included in any genetic analysis. Distributed in the Horn of Africa and the Arabian Peninsula, Hipposideros megalotis is the only Hipposiderid with a fold of skin joining the base of the ear pinnae. Its uniquely specialized auditory system and derived dentition (e.g., loss of anterior premolars and enlargement of outer lower incisors), led John Edwards Hill to regard it as a species that diverged early from the other groups of African Hipposideros. Including this species in future analyses would shed light on the group’s biogeography. Were there three colonizations of Africa by Asian groups of Hipposideros or could Hipposideros megalotis be sister to all Asian lineages of this genus? This information would greatly clarify ancestral geographic range inference.
The lineage delimitation analyses indicate that a number of Hipposiderid lineages are either unnamed or unidentified, and also that a number of recognized species may not be genetically and evolutionarily independent.
Previous studies had indicated that both Hipposideros caffer and Hipposideros ruber appear to be complexes of cryptic species. The two are traditionally distinguished on the basis of size and pelage colour, Hipposideros ruber being the larger and more brightly colored form, but this distinction is clouded by geographic variation in size and the presence of both reddish and gray-brown phases in both species. Our mitochondrial analyses identified four Hipposideros ruber lineages and eight Hipposideros caffer lineages in two distinct groupings among the sampled populations. Four of the caffer lineages and three of the ruber clades were identified as putative species by BPP analyses. The large number of clades in East Africa is remarkable: Kenya and Tanzania each support four of the eight clades allied with Hipposideros caffer, and all but one of the eight clades known from throughout the continent occur in one or the other East African country. This undoubtedly reflects the region’s great landscape diversity, where West and Central African rainforests reach their eastern limit, southern savannas reach their northern limits, the Sahel reaches its southern limits, and all are riven by the African Rift Valley. It also is a product of Patterson et al.'s sampling intensity.
Because some cyt-b sequences were used in multiple studies of this group, it is possible to relate Patterson et al.'s clade labels to those used by earlier studies. Based on attributions made on morphological grounds by previous studies, some well-supported but unnamed clades in our analysis can be identified. For instance, caffer1 has a distributional range and includes specimens previously identified as Hipposideros tephrus, while specimens of caffer4 come from near the type locality of Hipposideros caffer, and may well represent that species. However, no samples confidently identified as Hipposideros ruber from the vicinity of its type locality have been sequenced, leaving the application of that name to clades in any of these trees purely conjectural. Applying formal names only after integrative taxonomic assessment is a responsible course as multispecies coalescent models like BPP can lead to over-splitting of species, especially when applied to geographically variable species complexes with parapatric distributions.
Doryrhina is a poorly known genus characterised morphologically by the peculiar club-shaped processes on the central and posterior nose leaves. This trait is shared by the two recognized African species, Doryrhina cyclops and Doryrhina camerunensis, which differ chiefly in size (the latter is larger, with forearm lengths more than 75 mm). Although Doryrhina cyclops is considered to be monotypic, mitochondrial sequences clearly separate West African populations in Liberia and Senegal (cyclops1) from Central African populations in Gabon and Central African Republic (cyclops2), and these are substantially separated from Doryrhina camerunensis and a specimen referred to that species from Tanzania. However, both the intron analysis and the species tree show little or no geographic structure. The BPP analyses confirm that none of the mitochondrial clades is behaving as an independent evolutionary lineage. Geographic structure in mtDNA but continent-wide admixture in the nuclear genome could result from either male-biased dispersal with female philopatry or highly structured seasonal migrations, which are known in other Hipposiderids. In any case, the genetic patterns of Doryrhina are hard to reconcile with its space-use behavior; individuals appear to have very small home ranges, on the order of a few hectares. An integrative taxonomic review of the genus Doryrhina is needed to determine the validity of Doryrhina cyclops and Doryrhina camerunensis. It would also shed light on whether six Australo-Papuan species tentatively allocated to that genus belong there or elsewhere. George Tate had earlier allocated those species to the Australasian muscinus group, convergent on but separate from his Afrotropical cyclops group, but John Edwards Hill.
Patterson et al.'s analysis included four of the five recognized species of Macronycteris, lacking only Macronycteris thomensis, which is endemic to São Tomé Island in the Gulf of Guinea. Two species, Macronycteris gigas and Macronycteris vittata, occur on the African mainland and two others, Macronycteris commersoni and Macronycteris cryptovalorona, occur on Madagascar. Macronycteris cryptovalorona was named only in 2016, on the basis of its strong genetic divergence from Macronycteris cryptovalorona; appears as sister to all three remaining species of Macronycteris. Despite a search for diagnostic characters, a previous study led by Stephen Goodman could not distinguish it morphologically from Macronycteris commersoni. Both species are known to occur in the same caves in south central and southwestern Madagascar. On the other hand, Macronycteris vittata and Macronycteris gigas are distinguished typically on the basis of size and pelage colour. They are also known to occur together in the same cave, where they utilise echolocation calls with different peak frequencies: Macronycteris vittata at 64–70 kHz and Macronycteris gigas at 53.4–54.8 kHz. Both in Africa and on Madagascar, these pairs of taxa appear to act as distinct species, but the monophyly evident in the cyt-b sequences disappears in the nuclear intron analyses. BPP analyses fail to resolve any of the Macronycteris species, and none appear as monophyletic in the concatenated intron analyses.
Our results clearly underscore the importance of using multilocus datasets to evaluate phylogenetic and phylogeographic relationships at the genus and species level in Mammals. Use of a single genetic system may lead to widely divergent conclusions regarding species identity and distribution. David Toews and Alan Brelsford reviewed cases of mito-nuclear discordance in Animals generally. Fully 18% of the cases they reviewed had discordant patterns of mitochondrial and nuclear DNA. In most cases, such patterns are attributable to adaptive introgression of mtDNA, demographic disparities, and sex-biased asymmetries; in some cases they found evidence for hybrid zone movement or Human agency. Discordant patterns of variation between mitochondrial and nuclear DNA have been reported in at least six other families of Bats. A 2019 study led by Kanat Gürün implicated the role of sex-biased dispersal in causing such discordance, male dispersal spreading nuclear variation farther and faster than the movement of mitochondria. This may be a more general pattern in Bats. To understand the processes responsible for these discordant patterns of genome evolution, extensive genomic sampling and far fuller knowledge of natural history will be required.
See also...
