Relationships among lemur families

Relationships among lemur families have also proven to be problematic and have yet to be definitively resolved.^[15] To further complicate the issue, several Paleogene fossil primates from outside Madagascar, such as Bugtilemur, HP 533736-001 CPU FAN have been classified as lemurs.^[53] However, scientific consensus does not accept these assignments based on genetic evidence,^[15][52]and therefore it is generally accepted that the Malagasy primates are monophyletic.^[15][23][47] Another area of contention is the relationship between the sportive lemurs and the extinct koala lemurs (Megaladapidae). Formerly grouped in the same family due to similarities in dentition,^[54] they are no longer considered to be closely related due to genetic studies.^[47][55] HP 535438-001 CPU FAN More taxonomic changes have occurred at the genus level, although these revisions have proven more conclusive, often supported by genetic and molecular analysis. The most noticeable revisions included the gradual split of a broadly defined genus Lemur into separate genera for the ring-tailed lemur, ruffed lemurs, and brown lemurs due to a host of morphological differences.^[56][57] Due to several taxonomic revisions by Russell Mittermeier, HP 535439-001 CPU FAN Colin Groves, and others, the number of recognized lemur species has grown from 33 species and subspecies in 1994 to approximately 100 in 2008.^[30][42][58] With continuing cytogenetic andmolecular genetic research, as well as ongoing field studies, particularly with cryptic species such as mouse lemurs, the number of recognized lemur species is likely to keep growing.^[30] However, the rapid increase in the number of recognized species has had its critics among taxonomists and lemur researchers. HP 535441-001 CPU FAN Since classifications ultimately depend on the species concept used, conservationists often favor definitions that result in the splitting of genetically distinct populations into separate species to gain added environmental protection. Others favor a more thorough analysis. Lemurs vary greatly in size. They include the smallest primates in the world and, until recently, also included some of the largest. HP 535442-001 CPU FAN They currently range in size from about 30 g (1.1 oz) for Madame Berthe's mouse lemur (Microcebus berthae) up to 7–9 kg (15–20 lb) for the indri (Indri indri) and diademed sifaka(Propithecus diadema).^[59][60] When recently extinct species are considered, the size range extended up to that of a gorilla at 160–200 kg (350–440 lb) forArchaeoindris fontoynonti. Like all primates, lemurs have five divergent digits with nails (in most cases) on their hands and feet. HP 535766-001 CPU FAN Most lemurs possess a laterally compressed, elongated nail, called a toilet-claw, on the second toe and use it for scratching and grooming.^[50][61] In addition to the toilet-claw, lemurs share a variety of other traits with other strepsirrhine primates, which include a rhinarium (or "wet nose"); a fully functional vomeronasal organ, which detects pheromones; a postorbital barand the lack of postorbital closure (a wall of thin bone behind the eye); HP 537613-001 CPU FAN orbits (bony sockets that enclose the eye) that are not fully facing forward; left and right mandible (lower jaw) bones that are not fully fused; and a small brain-to-body mass ratio.^[14][62] Additional traits shared with other prosimian primates (strepsirrhine primates and tarsiers) include a bicornuate (two-horned) uterus and epitheliochorial placentation.^[12][62] HP 538340-001 CPU FAN Because their thumbs are only pseudo-opposable, making their movement less independent of the other fingers,^[61] their hands are less than perfect at grasping and manipulating objects.^[19] On their feet, they have a widely abducted hallux (first toe) which facilitates the grasping of tree limbs.^[50] A common misconception is that lemurs have a prehensile tail, a trait found only in New World monkeys, particularly atelids, among primates.^[61] HP 576837-001 CPU FAN Lemurs also rely heavily on their sense of smell, a trait shared with most other mammals and primitive primates, but not with the visually oriented higher primates.^[19] This sense of smell is important in terms of marking territory as well as provide an indication of whether or not another lemur is a viable breeding partner. Lemurs are a diverse group of primates in terms of morphology and physiology.^[30] HP 580696-001 CPU FAN Some lemurs, such as the sportive lemurs and indriids, have longer hind limbsthan forelimbs, making them excellent leapers.^[63][64][65] Indriids also have a specialized digestive system for folivory, exhibiting enlarged salivary glands, a spacious stomach, and an elongated caecum (lower gut) that facilitates fermentation.^[ The hairy-eared dwarf lemur (Allocebus trichotis) reportedly has a very long tongue, allowing it to feed on nectar.^[50] HP 580718-001 CPU FAN Likewise, the red-bellied lemur (Eulemur rubriventer) has a feathery brush-shaped tongue, also uniquely adapted to feed on nectar and pollen.^[11] The aye-aye has evolved some traits that are unique among primates, making it stand out among the lemurs. Such traits include continuously growing, rodent-like front teeth for gnawing through wood and hard seeds; a highly mobile, filiform (filament-shaped) middle finger for extracting food from tiny holes; HP 582139-001 CPU FAN large, bat-like ears for detecting hollow spaces within trees; and use of self-generated acoustical cues to forage.^[49] Lemurs are unusual since they have great variability in their social structure, yet generally lack sexual dimorphism in size and canine tooth morphology.^[11][39]However, some species tend towards having larger females,^[49] and two species of true lemur (genus Eulemur), the gray-headed lemur (E. albocollaris) and the red lemur (E. rufus), exhibit size differences in canine teeth.^[69] HP 582141-001 CPU FAN True lemurs show sexual dichromatism (sexual differences in fur coloration),^[39] but the difference between the genders varies from strikingly obvious, as in the blue-eyed black lemur (E. macaco), to nearly imperceptible in the case of the common brown lemur (E. fulvus).^[69] Crypsis, or the inability of humans to visually distinguish between two or more distinct species, has recently been discovered among lemurs, particularly within the sportive lemurs (Lepilemur) and mouse lemurs (Microcebus). HP 602472-001 CPU FAN With sportive lemurs, subspecies were traditionally defined based on slight morphological differences, but new genetic evidence has supported giving full species status to these regional populations.^[55] In the case of mouse lemurs, the gray mouse lemur (M. murinus), golden-brown mouse lemur (M. ravelobensis), and Goodman's mouse lemur (M. lehilahytsara) were considered the same species until recently, when genetic tests identified them as cryptic species. HP 603690-001 CPU FAN The lemur dentition is heterodont (having multiple tooth morphologies) and derives from an ancestral primate permanent dentition of 2.1.3.32.1.3.3. Indriids, sportive lemurs, the aye-aye, and the extinctsloth lemurs, monkey lemurs, and koala lemurs have reduced dentitions, having lost incisors, canines, or premolars.^[75] The ancestral deciduous dentitionis 2.1.32.1.3, but young indriids, aye-ayes, koala lemurs, sloth lemurs, and probably monkey lemurs have fewer deciduous teeth.^[54][71] HP 603691-001 CPU FAN There are also noticeable differences in dental morphology and tooth topography between lemurs.Indri, for instance, have teeth that are perfectly adapted for shearing leaves and crushing seeds.^[60] In the toothcomb of most lemurs, the bottom incisors and canine teeth are procumbent (face forward rather than up) and finely spaced, thus providing a tool for either grooming or feeding.^[14][54][75] For instance, indri use their toothcomb not only for grooming, HP 6043B0034801A0​2 CPU FAN but also to pry out the large seeds from the tough exocarp of Beilschmiedia fruits,^[76] while fork-marked lemurs use their relatively long toothcomb to cut through tree bark to induce the flow of tree sap.^[50] The toothcomb is kept clean by the sublingua or "under-tongue", a specialized structure that acts like a toothbrush to remove hair and other debris. The sublingua extends below the tip of the tongue and is tipped with keratinized, serrated points that rake between the front teeth. HP 606013-001 CPU FAN Only the aye-aye, the extinct giant aye-aye, and the largest of the extinct giant sloth lemurs lack a functional strepsirrhine toothcomb.^[75][73] In the case of the aye-aye, the morphology of the deciduous incisors, which are lost shortly after birth, indicate that its ancestors had a toothcomb. These milk teeth are lost shortly after birth^[79] and are replaced by open-rooted, continually growing (hypselodont) incisors.^[75] The toothcomb in lemurs normally consists of six teeth (four incisors HP 606574-001 CPU FAN and two canines), although indriids, monkey lemurs, and some sloth lemurs only have a four-tooth toothcomb due to the loss of either a canine or an incisor.^[14][75] Because the lower canine is either included in the toothcomb or lost, the lower dentition can be difficult to read, especially since the first premolar (P2) is often shaped like a canine (caniniform) to fill the canine's role.^[54] In folivorous (leaf-eating) lemurs, except for indriids, the upper incisors are greatly reduced or absent.^[54][75] HP 606575-001 CPU FAN Used together with the toothcomb on themandible (lower jaw), this complex is reminiscent of an ungulate browsing pad.^[75] Lemurs are unusual among primates for their rapid dental development, particularly among the largest species. For example, indriids have relatively slow body growth but extremely fast tooth formation and eruption.^[80] By contrast, anthropoidprimates exhibit slower dental development with increased size and slower morphological development.^[75] HP 606609-001 CPU FAN Lemurs are also dentally precocious at birth, and have their full permanent dentition at weaning.^[29] Lemurs generally have thin tooth enamel compared to anthropoid primates. This may result in extra wear and breakage to the anterior (front) teeth due to heavy use in grooming, feeding, and fighting. Little other dental health information is available for lemurs, HP 608378-001 CPU FAN except that wild ring-tailed lemurs at Berenty Private Reserve occasionally exhibit abscessed maxillary canines (seen as open wounds on the muzzle) and tooth decay, possibly due to the consumption of non-native foods. The sense of smell, or olfaction, is highly important to lemurs and is frequently used in communication.^[11][13][19] Lemurs have long snouts (compared to the short snouts of haplorrhines) that are traditionally thought to position the nose for better sifting of smells,^[13] HP 608772-001 CPU FAN although long snouts do not necessarily translate into high olfactory acuity since its not the relative size of the nasal cavity that correlates with smell, but the density of olfactory receptors.^[81][82] Instead, the long snouts may facilitate better chewing. The wet nose, or rhinarium, is a trait shared with other strepsirrhines and many other mammals, but not with haplorrhine primates.^[50] HP 610773-001 CPU FAN Although it is claimed to enhance the sense of smell,^[62] it is actually a touch-based sense organ that connects with a well-developed vomeronasal organ (VNO). Since pheromones are usually large, non-volatile molecules, the rhinarium is used to touch a scent-marked object and transfer the pheromone molecules down the philtrum (the nasal mid-line cleft) to the VNO via the nasopalatine ducts that travel through the incisive foramen of the hard palate.^[12] HP 610774-001 CPU FAN To communicate with smell, which is useful at night, lemurs will scent mark with urine as well as scent glands located on the wrists, inside elbow, genital regions, or the neck.^[12][62] The scrotal skin of most male lemurs has scent glands.^[83] Ruffed lemurs (genus Varecia) and male sifakas have a gland at the base of their neck,^[12][50] while the greater bamboo lemur(Prolemur simus) and the ring-tailed lemur have glands inside the upper arms near the axilla.^[12] HP 610777-001 CPU FAN Male ring-tailed lemurs also have scent glands on the inside of their forearms, adjacent to a thorn-like spur, which they use to gouge, and simultaneously, scent-mark tree branches.^[50] They will also wipe their tails between their forearms and then engage in "stink fights" by waving their tail as their opponents.^[12] Lemurs (and strepsirrhines in general) are considered to be less visually oriented than the higher primates, since they rely so heavily on their sense of smell and pheromone detection. HP 622028-001 CPU FAN The fovea on the retina; which yields higher visual acuity, is not well-developed. The postorbital septum (or bony closure behind the eye) in haplorrhine primates is thought to stabilize the eye slightly, allowing for the evolution of the fovea. With only a postorbital bar, lemurs have been unable to develop a fovea.^[84] Therefore, regardless of their activity pattern (nocturnal, cathemeral, or diurnal), lemurs exhibit low visual acuity and high retinal summation.^[29] HP 622029-001 CPU FAN Lemurs can see a wider visual field, however, than anthropoid primates due to a slight difference in the angle between the eyes. Although they lack a fovea, some diurnal lemurs have a cone-rich, although less clustered, area centralis.^[84] This area centralis has a high rod-to-cone cell ratio in many diurnal species studied thus far, whereas diurnal anthropoids have no rod cells in their fovea. Once again, this suggests lower visual acuity in lemurs than in anthropoids.^[86] HP 622330-001 CPU FAN Furthermore, the rod-to-cone cell ratio can be variable even among diurnal species. For instance, Verreaux's sifaka (Propithecus verreauxi) and the indri (Indri indri) have only a few large cones scattered along their predominantly rod-dominated retina. The eyes of the ring-tailed lemur contain one cone to five rods. Nocturnal lemurs such as mouse lemurs and dwarf lemurs, on the other hand, have retinas made up entirely of rod cells.^[12] HP 637607-001 CPU FAN Since cone cells make color vision possible, the high prevalence of rod cells in lemur eyes suggest they have not evolved color vision.^[12] The most studied lemur, the ring-tailed lemur, has been shown to have blue-yellow vision, but lacks the ability to distinguish red and green hues.^[87] Due to polymorphism inopsin genes, which code for color receptivity, trichromatic vision may rarely occur in females of a few lemur species, such as Coquerel's sifaka (Propithecus coquereli) and the red ruffed lemur (Varecia rubra). HP 646578-001 CPU FAN Most lemurs, therefore, are either monochromats or dichromats. Most lemurs have retained the tapetum lucidum, a reflective layer of tissue in the eye, which is found in many vertebrates.^[39] This trait is absent in haplorrhine primates, and its presence further limits the visual acuity in lemurs.^[29][86] The strepsirrhine choroidal tapetum is unique among mammals because it is made up of crystalline riboflavin, and the resulting optical scattering is what limits visual acuity.^[86] HP 657529-001 CPU FAN