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s, the smallest primates in the world, evolved in isolation along with other lemurs on the island of Madagascar.]] The evolutionary history of lemurs occurred in isolation from other primates on the island of Madagascar for at least 40 million years. Lemurs are prosimian primates belonging to the suborder Strepsirrhini, which branched off from other primates less than 63 mya (million years ago). They share some traits with the most basal primates, and thus are often confused as being ancestral to modern monkeys, apes, and humans. Instead, they merely resemble ancestral primates.

Lemurs are thought to have evolved during the Eocene or earlier, sharing a closest common ancestor with lorisiforms. Fossils from Africa and tests of nuclear DNA suggest that lemurs made their way to Madagascar between 40 and 52 mya. Molecular tests offer an alternative date range of 62 to 65 mya. An ancestral lemur population is thought to have inadvertently rafted to the island on a floating mat of vegetation, although hypotheses for land bridges and island hopping have also been proposed. The timing and number of hypothesized colonizations has traditionally hinged on the phylogenetic affinities of the Aye-aye, the most basal member of the lemur clade.

Having undergone their own independent evolution on Madagascar, lemurs have diversified to fill many niches normally filled by other types of mammals. They include the smallest primates in the world, and once included some of the largest. Since the arrival of humans approximately 2,000 years ago, they are now restricted to 10% of the island, or approximately 60,000 square kilometres (23,000 sq mi), and many are facing extinction. For this reason, researchers have been trying to identify and assess every species. Over the last 10 to 20 years, there has been a steep increase in the number of recognized lemur species and subspecies, both through the discovery of new species and the elevation of existing subspecies to full species status. Currently there are approximately 100 or more recognized species or subspecies of living lemur, which are divided into five families and 15 genera. If the extinct subfossil lemurs are included, an additional three families, eight genera, and 17 species would be included. The recent rise in species numbers is due to both improved genetic analysis and a push in conservation to encourage the protection of isolated and distinct lemur populations. Not everyone in the scientific community supports these taxonomic changes, with some preferring instead an estimate of 50 living species.

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Evolutionary history

Lemurs are prosimian primates belonging to the suborder Strepsirrhini. Like other strepsirrhine primates, such as lorises, pottos, and galagos, they share ancestral traits with early primates. In this regard, lemurs are popularly confused with ancestral primates; however, lemurs did not give rise to monkeys and apes, but evolved independently on Madagascar.[1]

, a trait shared by lemurs with their closest relatives, the lorises, weighs heavily on the evolutionary history of strepsirrhines and the lemur colonization of Madagascar.]] Primates first evolved sometime between the Middle Cretaceous and the early Paleocene periods on either the supercontinent of Laurasia or in Africa.[2] According to molecular clock studies, the last common ancestor of all primates dates to around 79.6 mya,[3] although the earliest known fossil primates are only 54–55 mya old.[4] The closest relatives of primates are the extinct plesiadapiforms, the modern colugos (commonly and inaccurately named "flying lemurs"), and treeshrews.[3] Some of the earliest known true primates are represented by the fossil groups Omomyidae, Eosimiidae, and Adapiformes.

The relationship between known fossil primate families remains unclear. A conservative estimate for the divergence of haplorrhines (tarsiers, monkeys, apes, and humans) and strepsirrhines is 58 to 63 mya,[5] and a consensus is emerging that places tarsiers close to omomyids, while eosimids gave rise to the simians (non-tarsier haplorrhines) and the adapiforms gave rise to modern strepsirrhines, including lemurs.[6] In 2009, a highly publicized and scientifically criticized publication proclaimed that a 47 million-year-old adapiform fossil, Darwinius masillae, demonstrated both adapiform and simian traits, making it a transitional form between the prosimian and simian lineages.[7] Media sources inaccurately dubbed the fossil as a "missing link" between lemurs and humans.[8]

Lemurs are currently thought to have evolved during the Eocene (37 to 55 mya),[5][9] although molecular tests suggest the Paleocene (65 to 56 mya) or later.[9] Until recently, they were thought to have descended directly from the diverse group of adapiforms due to several shared postcranial traits,[10] as well as long snouts and small brains. Although adapiforms also had lemur-like auditory bullae, a prosimian characteristic,[11] they had smaller brains and longer snouts than lemurs.[12] There are also several other morphological differences. Most noticeably, adapiforms lack a key derived trait, the strepsirrhine toothcomb, and possibly the toilet-claw, found not only in strepsirrhines but also in tarsiers. Unlike lemurs, adapiforms exhibited a fused mandibular symphysis (a characteristic of simians) and also possessed four premolars, instead of three or two.[13]

Comparative studies of the cytochrome b gene, which are frequently used to determine phylogenetic relationships among mammals—particularly within families and genera[14]—have been used to show that lemurs share common ancestry with lorisiforms.[13][15] This conclusion is also corroborated by the shared strepsirhine toothcomb, an unusual trait that is unlikely to have evolved twice.[16] If adapiforms were the ancestors of the living strepsirrhines, then the first strepsirrhines would have to predate the early Eocene, a view supported by molecular phylogenetic studies,[13] which show that lemurs split from lorises approximately 62 to 65 mya.[17] The molecular studies also show that lemuriforms diversified before the modern lorisiforms.[13] Using only nuclear genes, another study dated the split between lemurs and lorises at 60 mya, lemur diversification at 50 mya, and the lemur colonization of Madagascar somewhere between these two approximate dates.[18]

The fossil record tells a different story. Although it can only show the earliest possible date for the appearance of a taxonomic group, other concerns have arisen about these vastly earlier divergence dates predicted independently of the fossil record. First, palaeontologists have expressed concerns that if primates have been around for significantly more than 65 million years, then the first one-third of the primate fossil record is missing. Another problem is that some of the these molecular dates have overestimated the divergence of other mammalian orders, such as Rodentia, suggesting primate divergence might also be overestimated. Currently the oldest known strepsirrhine, Djebelemur, dates from the early Eocene in northern Africa and lacks a fully differentiated toothcomb. Based on fossils and other genetic tests, a more conservative estimate dates the divergence between lemurs and lorises to around 50 to 55 mya.[5]

To complicate the ancestry puzzle, no terrestrial Eocene or Paleocene fossils have been found on Madagascar,[19][20] and the fossil record from both Africa and Asia around this time is not much better.[13] Fossil sites in Madagascar are restricted to only five windows in time, which omit most of the Cenozoic, from 65 mya to ~26,000 years ago. What little fossil-bearing rock exists from this vast span of time is dominated by marine strata along the west coast.[21] The oldest lemur fossils on Madagascar are actually subfossils dating to the Late Pleistocene.[10]

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Colonization of Madagascar

Once part of the supercontinent Gondwana, Madagascar broke away from eastern Africa, the likely source of the ancestral lemur population, about 160 mya and then from Antarctica between 80 and 130 mya. Initially, the island drifted south from where it split from Africa (around modern Somalia) until it reached its current position between 80 and 90 mya. Around that time, it split with India, leaving it isolated in the Indian Ocean and separated from nearby Africa by the Mozambique Channel,[22][23] a deep channel with a minimum width of approximately 560 kilometers (350 mi).[13] These separation dates and the estimated age of the primate lineage preclude any possibility that lemurs could have been on the island before the Madagascar pulled away from Africa.[24] In support of this, mammalian fossils on Madagascar from the Cretaceous (see Mesozoic mammals of Madagascar) include gondwanatheres and other mammalian groups that would not have been ancestral to lemurs or the other endemic mammals present on the island today.[13]


With Madagascar already geographically isolated by the Paleocene and lemur diversification dating to the same time, an explanation was needed for how lemurs had made it to the island. In the 19th century, prior to the theory of continental drift, scientists including Philip Sclater, Étienne Geoffroy Saint-Hilaire, and Ernst Haeckel suggested that Madagascar and India were once part of a southern continent—named Lemuria by Sclater—that has since disappeared under the Indian Ocean.[25][26] By the early 20th century, oceanic dispersal emerged as the most popular explanation for how lemurs reached the island.[21][23][27] The idea first took shape under the anti-plate tectonics movement of the early 1900s, when renowned paleontologist William Diller Matthew proposed the idea in his influential article "Climate and Evolution" in 1915. In the article, Matthew could only account for the presence of lemurs in Madagascar by "rafting".[28] Although unlikely, over long periods of time terrestrial animals can occasionally raft to remote islands on floating mats of tangled vegetation, which get flushed out to sea from major rivers by floodwaters.[13][28][29] In the 1940s, American paleontologist George Gaylord Simpson coined the term "sweepstakes dispersal" for such unlikely events. Today, a rafting event remains the most accepted explanation for the lemur colonization of Madagascar.[30]

Any extended ocean voyage without fresh water or food would prove difficult for a large, warm-blooded (or "homeothermic") mammal, but today many small, nocturnal species of lemur exhibit heterothermy, which allows them to lower their metabolism and become dormant while living off fat reserves. Such a trait in a small, nocturnal lemur ancestor would have facilitated the ocean voyage and could have been passed on to its descendants.[29] However, this trait has not been observed in the closely-related lorisiforms studied to date, and could have evolved on Madagascar in response to the island's harsh environmental conditions.[13]

Because only five terrestrial orders of mammals have made it to the island, each likely to have derived from a single colonization,[24] and since these colonizations date to either the early Cenozoic or the early Miocene, the conditions for oceanic dispersal to Madagascar seem to have been better during two separate periods in the past.[13] A report published in January 2010 supported this assumption by demonstrating that both Madagascar and Africa were 1,650 km (1,030 mi) south of their present-day positions around 60 mya, placing them in a different ocean gyre and reversing the strong current that presently flows away from Madagascar. The currents were even shown to be stronger than they are today, shortening the rafting time to approximately 30 days or less, making the crossing much easier for a small mammal. Over time, as the continental plates drifted northward, the currents gradually changed, and by 20 mya the window for oceanic dispersal had closed.[31]

Since the 1970s, the rafting hypothesis has been called into question by claims that lemur family Cheirogaleidae might be more closely related to the other Afro-Asian strepsirrhines than to the rest of the lemurs. This idea was initially based on similarities in behavior and molar morphology, although it gained support with the 2001 discovery of 30 million-year-old Bugtilemur in Pakistan and the 2003 discovery of 40 million-year-old Karanisia in Egypt. Karanisia is the oldest fossil found that bears a toothcomb, whereas Bugtilemur was thought to have a toothcomb, but also had even more similar molar morphology to Cheirogaleus (dwarf lemurs). If these relationships had been correct, the dates of these fossils would have had implications on the colonization of Madagascar, requiring two separate events. The most parsimonious explanation, given the genetic evidence and the absence of toothcombed primates in European fossil sites,[13] is that stem strepsirrhines evolved on the Afro-Arabian landmass, dispersing to Madagascar and more recently from Africa to Asia.[32] More recently, the structure and general presence of the toothcomb in Bugtilemur has been questioned, as well as many other dental features, suggesting it is most likely an adapiform.[5]

An alternative form of oceanic dispersal that had been considered was island hopping, where the lemur ancestors might have made it to Madagascar in small steps by colonizing exposed seamounts during times of low sea level.[12][21] However, this is unlikely since the only seamounts found along the Davie Ridge would have been too small in a such a wide channel. Even though the Comoros Islands between Africa and Madagascar are significantly larger, they are too young, having been formed by volcanic activity only around 8 mya.[21] A land bridge between Madagascar and Africa has also been proposed, but a land bridge would have facilitated the migration of a much greater sampling of Africa's mammalian fauna than is endemic to the island. Furthermore, deep trenches separate Madagascar from the mainland, and prior to the Oligocene, sea level was significantly higher than today.[33]

Despite these issues, one variant of the land bridge hypothesis may best explain both how a land bridge could have formed, and how it other mammalian orders failed to cross it.[5] Geological studies have shown that following the collision of India and Asia, the Davie Fracture Zone had been pushed up by tectonic forces, possibly high enough to create a land bridge. Indeed, core samples along the Davie Fracture Zone suggest that at least parts of the Mozambique Channel were above sea level between 45 and 26 mya,[34] or possibly as early as 55 mya.[5] Following the Indian-Asian collision, the fault type changed from a strike-slip fault to a normal fault, and seafloor spreading created compression along the Davie Fracture Zone, causing it to rise. By the early Miocene, the East African Rift created tension along the fault, causing it to subside beneath the ocean. Coinciding with this, the divergence dates of nearly all the Malagasy mammalian orders fall within this window. Old World monkeys, dogs, and cats did not diverge or arrive in Africa until later in the Miocene.[34] Still, more recent dating of divergence of the Malagasy mammalian clades falls outside of this land bridge window, and a much greater diversity of mammal groups would be expected on Madagascar had the land bridge been present during that stretch of time.[18]

The dating of the lemur colonization is controversial for the same reasons as that of strepsirrhine evolution. Using molecular testing, the colonization has been estimated at 62 to 65 mya based on the split between the Aye-aye and the rest of the lemurs.[17] On the other hand, the sparse fossil record and estimates based on nuclear genes support a more conservative estimate of 40 to 52 mya.[5] Once safely established on Madagascar, with its limited mammalian population, the lemurs were protected from the increasing competition from evolving arboreal mammalian groups.[19] Monkeys had evolved by the Oligocene, and their intelligence, aggression, and deceptiveness may have given them the advantage in exploiting the environment over the diurnal adapiform primates in Africa and Asia, ultimately driving them to extinction, leaving only the nocturnal lorisiforms.[12][35]

Diversification

The ancestral lemur that colonized Madagascar is thought to have been small and nocturnal.[36] More specifically, it is thought to have had adapiform-like cranial anatomy—particularly the cranial foramina and the middle ear—comparable to that of lemurids, while being similar to cheirogaleids in dentition and postcranial anatomy.[5] Lemurs have since diversified greatly, starting with the Aye-aye and its extinct relations, whose divergence is popularly thought to have occurred shortly after the lemur colonization of Madagascar.[17] According to molecular studies, there have since been two major episodes of diversification, from which all other known extant and extinct family lineages emerged. The remaining families diverged during a 10 to 12 million-year window, between the Late Eocene (42 mya) and into the Oligocene (30 mya).[17][27] In fact, these dates for this divergence window coincided with the Eocene-Oligocene extinction event, during which time climate cooling took place and changes in ocean currents altered weather patterns.[17][5] Outside of Madagascar, these dates also coincide with the divergence of the lorisiform primates and five major clades of squirrels, all occupying similar niches as lemurs.[17] The dates do not suggest that increased predation drove family-level divergence since the first carnivores arrived on the island between 24 and 18 mya.[36]

The second major episode of diversification occurred during the Late Miocene, approximately 8 to 12 mya, and included the true lemurs (Eulemur) and the mouse lemurs (Microcebus).[17][27] In both the true lemurs and mouse lemurs, their populations were thought to have diverged due to habitat fragmentation caused when humans arrived on the island roughly 2,000 years ago.[10] Only recently has molecular research started to show a more distant split in these genera.[37] Most surprising were the mouse lemurs, a group which is now thought to contain cryptic species, meaning they are indistinguishable from each other based solely on appearance. In contrast, true lemurs are easier to distinguish and exhibit sexual dichromatism.[17] Studies in karyology, molecular genetics, and biogeographic patterns have also assisted in understanding their phylogeny and diversification.[37] Although the divergence times for these two genera are imprecise, this estimated divergence time would overlap with a change to a wetter climate in Madagascar, as new weather patterns generated monsoons and likely influenced the plant life.[17][27]

This difference in evolutionary divergence between the two genera may be due to differences in their activity patterns. True lemurs are often diurnal, allowing sexual partners to distinguish each other as well as other related species visually. Mouse lemurs, on the other hand, are nocturnal, reducing their ability to use visual signals for mate selection. Instead, they use olfactory and auditory signaling. For these reasons, true lemurs may have evolved sexual dichromatism while mouse lemurs evolved to be cryptic species.[17]

Distribution and diversity

Since their arrival on Madagascar, lemurs have diversified both in behavior and morphology. Their diversity rivals that of the monkeys and apes found throughout the rest of the world, especially when the recently extinct subfossil lemurs are considered.[35] Ranging in size from the 30 g (1.1 oz) Madame Berthe's Mouse Lemur, the world's smallest primate,[38] to the extinct Template:Convert/– Archaeoindris fontoynonti,[39] lemurs evolved diverse forms of locomotion, varying levels of social complexity, and unique adaptations to the local climate. Until recently, they had gone on to fill many niches normally occupied by monkeys, squirrels, woodpeckers, and large grazing ungulates.[12][19] In addition to the incredible diversity between lemur families, there has also been great diversification among closely-related lemurs. Yet despite separation by geographical barriers or by niche differentiation in sympatry, occasionally hybridization can occur.[35] Lemur diversification has also created generalist species, such as the true lemurs of northern Madagascar, which are very adaptable, mostly nondescript, and found throughout most of the island's forests.[10]

[[File:|thumb|left|alt=A Diademed Sifaka (a lemur with black and gray back; white and black head; orange limbs; black hands; and long legs and tail) clinging to a tree.|The Diademed Sifaka (Propithecus diadema) is one of the largest of the living lemurs, comparable in size to the Indri. It lives in the rainforests of Madagascar and eats a varied diet of leaves and fruit.]] Most of the 99 living lemur taxa are found only on Madagascar. Two species, the Common Brown Lemur (Eulemur fulvus) and the Mongoose Lemur (Eulemur mongoz), can also be found on the Comoro Islands, although it is assumed that both species were introduced to the islands from northwestern Madagascar by humans within the last few hundred years.[40][41] Molecular studies on Eulemur fulvus fulvus (from the mainland) and E. f. mayottensis (from the Comoro Islands)[24] and on Comoro and mainland Mongoose Lemurs have supported this assumption by showing no genetic differences between the two populations.[41] Because all lemurs, including these two brown lemur species, are only native to the island of Madagascar, they are considered to be endemic.

Historically, lemurs ranged across the entire island inhabiting a wide variety of habitats, including dry deciduous forests, lowland forests, spiny thickets, subhumid forests, montane forest, and mangrove. Today, their collective range is restricted to 10% of the island, or approximately 60,000 km2 (23,000 sq mi).[42] Most of the remaining forests and lemurs are found along the periphery of the island. The center of the island, the Hauts Plateaux ("High Plateaus"), was converted by early settlers to rice paddies and grassland through slash-and-burn agriculture, known locally as tavy. As erosion depleted the soil, the cyclical forest regrowth and burning ended as the forest gradually failed to return.[43] Today, the level of floral diversity increases with precipitation, from the dry southern forests to the wetter norther forests to the rainforests along the east coast. Increased foliage corresponds to increased faunal diversity, including the diversity and complexity of lemur communities.[10]

Having evolved in Madagascar's challenging environment, replete with poor soils, extreme shifts in poor, seasonal plant productivity, and devastating climatic events such as extended droughts and annual cyclones,[9] lemurs have adopted unique combinations of unusual traits to survive, distinguishing them significantly from other primates. In response to limited, seasonal resources, lemurs may exhibit seasonal fat storage, hypometabolism (including torpor and hibernation in some cheirogaleids), small group sizes, low encephalization (relative brain size), cathemerality (activity both day and night), and/or strict breeding seasons.[9][44] Secondarily, extreme resource limitations and seasonal breeding are thought to have resulted in three other relatively common lemur traits: female dominance, sexual monomorphism (lack of size differences between the sexes), and male-male competition for mates involving low levels of agonism (conflict), such as sperm competition.[45]

The arrival of humans on the island 1,500 to 2,000 years ago has taken a significant toll, not only on the size of lemur populations, but also on their diversity.[19] Due to habitat destruction and hunting, at least 17 species and 8 genera have gone extinct and the populations of all species have decreased.[39][46] A couple of species once thought to have gone extinct have since been rediscovered. The Hairy-eared Dwarf Lemur (Allocebus trichotis) was only known from five museum specimens, most collected in the late 19th century and one in 1965. It was rediscovered in 1989[47] and has since been identified in five national parks, although it is very rare within its range.[38] Likewise, the Greater Bamboo Lemur (Prolemur simus) was thought to be extinct as recently as the late 1970s, but a population was located near Ranomafana National Park in the late 1980s.[48] Historically, it had a much wider geographic distribution, shown by subfossil remains, but today it remains one of the world's 25 most endangered primates.[48][49][50][51] One distinctive morph (possibly a species or subspecies) of sifaka,[N 1] has not been so fortunate, having been extirpated from all known localities.[54] Unless trends change, extinctions are likely to continue.[55]

that went extinct less than a thousand years ago.]]

Until recently, giant species of lemur existed on Madagascar. Now represented only by recent or subfossil remains, they were modern forms and are counted as part of the rich lemur diversity that has evolved in isolation. Some of their adaptations were unlike those seen in lemurs today.[19] All 17 extinct lemurs were larger than the extant forms, some weighing as much as 200 kg (440 lb),[35] and are thought to have been active during the day.[56] Not only were they unlike the living lemurs in both size and appearance, they also filled ecological niches that no longer exist or are now left unoccupied.[19] Large parts of Madagascar, which are now devoid of forests and lemurs, once hosted diverse primate communities that included more than 20 species covering the full range of lemur sizes.[57]

Taxonomic and phylogenetic classification

Lemur taxonomy is controversial, and not all experts agree, particularly with the recent increase in the number of recognized species.[58][59][60] According to Russell Mittermeier, the president of Conservation International (CI), taxonomist Colin Groves, and others, there are currently 99 recognized species or subspecies of extant lemur, divided into five families and 15 genera.[61] Conversely, other experts in the field label this as a possible example of taxonomic inflation,[60] and prefer instead an estimate of at least 50 species.[58] All sides generally agree that the recently extinct subfossil lemurs should be classified in three families, eight genera, and 17 species.[39][46]

Closest lemur relations[3]
Euarchonta 

Scandentia (treeshrews)




Dermoptera (colugos)




Plesiadapiformes


 Primates 

Haplorrhini (tarsiers, monkeys, apes)


 Strepsirrhini 

Lorises, pottos, and galagos



Lemurs







Since the first taxonomic classification of lemurs in 1758 by Carl Linnaeus, many changes have been made to lemur taxonomy. Within the order Primates, treeshrews (order Scandentia) were considered basal, prosimian primates—close relatives of lemurs—until the 1980s.[62] Colugos, also incorrectly referred to as "flying lemurs", were once considered lemur-like primates, but were reclassified as close relatives of bats,[63] and more recently as close relatives of primates within their own order, Dermoptera.[3] Primates, together with their closest relatives, the treeshrews, colugos, and long-extinct plesiadapiforms, form the taxonomically unranked Euarchonta clade within the Euarchontoglires. Also, all lorisids originally placed in the genus Lemur by Carl Linnaeus have since been moved into either their own infraorder (Lorisiformes) or their own superfamily (Lorisoidea) within Lemuriformes.[64][5]

For the Malagasy primate fauna, taxonomic nomenclature proliferated during the 1800s, with the aid of museum systematists, such as Albert Günther and John Edward Gray, as well as naturalists and explorers, such as Alfred Grandidier and Alphonse Milne-Edwards.[65][66] The taxonomic nomenclature of lemurs was not sorted out until decades later, when Ernst Schwarz standardized it in 1931.[65][66][67] It was not until the 1990s that this nomenclature started to see a new wave of taxonomic change.[60]

Suprageneric classification

Since the 19th century, the classification of lemurs above the genus level has seen many changes. Early taxonomists proposed a variety of classifications for lemurs, but generally separated indriids from other lemurs and placed the Aye-aye in a major group of its own; some classified the dwarf and mouse lemurs with the galagos.[68] In 1915, William King Gregory published a classification[69] that remained generally accepted over the next decades. He placed all the lemurs together in a "series" Lemuriformes and recognized three families: Daubentoniidae, Indriidae, and Lemuridae (including the current Cheirogaleidae and Lepilemuridae).[68] George Gaylord Simpson's influential 1945 classification of mammals placed the treeshrews and the fossil Anagale (both now classified outside Primates) inside Lemuriformes and classified the fossil families Plesiadapidae and Adapidae in a superfamily Lemuroidea with most of the lemurs.[70]

Although treeshrews, plesiadapids, and the like are now no longer considered to be closely related to lemurs, disagreements persist over the classification of lemurs and related groups, resulting in two competing arrangements of the infraorders and superfamilies within Strepsirrhini. Colin Groves, in the 2005 third edition of Mammal Species of the World, classifies living strepsirrhines under three infraorders and two superfamilies. This places the Aye-aye within its own infraorder, separate from both lemurs (divided into two superfamilies) and lorises.[64] Since the publication of Mammal Species of the World, there has been little support in the academic literature for placing the Aye-aye in its own infraorder, and more recently Mittermeier, Groves, and other editors have ignored this taxonomic level.[61] An alternative classification draws the lines for infraorders and superfamilies differently, though using the same general phylogenetic tree. It classifies all living strepsirrhines under one infraorder, with the lorises and lemurs in separate superfamilies.[5]

Two alternative lemur classifications at the infraorder and superfamily levels
3 infraorders, 2 superfamilies[64] 1 infraorder, 2 superfamilies[5][71]

The classification of several lemur taxa has elicited particular debate. Most significantly, the placement of the Aye-aye has been controversial since its introduction to Western science in 1782, and it has been a topic of debate up until very recently.[35][72][68] Hinged upon morphological traits and molecular data, it has had profound implications on scientific theories.[72] Arguing against Darwin's theory of natural selection, Richard Owen claimed in 1863 that the Aye-aye's distinct characteristics, including its ever-growing incisors and unique, highly flexible middle finger, are so perfectly adapted for their uses in extractive foraging that they could not have evolved gradually through natural selection.[72] More recently, the Aye-aye's placement within the order Primates has posed problems for the rafting hypothesis for the primate colonization of Madagascar. If this species does not form a monophyletic group with the rest of the lemurs, then multiple colonization events would have had to occur to explain the present-day distribution of non-human primates on Madagascar.[35]

File:Aye-aye (Daubentonia madagascariensis)
The Aye-aye has traditionally been difficult to classify due to its unique physical traits.

Until Richard Owen published a definitive anatomical study in 1866, early naturalists were uncertain whether the Aye-aye (genus Daubentonia) was a primate, rodent, or marsupial.[72][73][74] In the late eighteenth century, for example, the Aye-aye was classified under the squirrel genus Sciurus.[75] By emphasizing its primate features, such as its postorbital bar, stereoscopic vision, and opposable hallux, over its rodent-like teeth, Owen demonstrated its affinity with other primates.[72][76] In 1996, Ankel-Simons demonstrated that the shape and arrangement of the Aye-aye's diminutive deciduous incisors indicate that this genus has a shared ancestry with the toothcombed primates.[16] However, the placement of the Aye-aye within the order Primates remained problematic until very recently. The karyotype of the Aye-aye is noticeably different from that of its closest relatives, the lorises and the rest of the lemurs, with a diploid chromosome count of 2n=30.[77] Based on its anatomy, researchers have found support for classifying the genus Daubentonia as a specialized indriid, a monotypic sister group to all strepsirrhines, and an indeterminate taxon within the order Primates.[15] In 1931, Schwarz labeled the Aye-aye as an offshoot of Indriidae, claiming that all lemurs were monophyletic, whereas Reginald Innes Pocock had previously placed the Aye-aye outside of the lemurs.[67] In that same year, Anthony and Coupin classified the Aye-aye under infraorder Chiromyiformes, a sister group to the other strepsirrhines. Colin Groves upheld this classification in 2005 because he was not entirely convinced the Aye-aye formed a clade with the rest of the Malagasy lemurs,[78] despite molecular tests that had shown Daubentoniidae was basal to all Lemuriformes.[15][79] In 2008, Russell Mittermeier, Colin Groves, and others ignored addressing higher-level taxonomy by defining lemurs as monophyletic and containing five living families, including Daubentoniidae.[61]

Another interpretation of the Aye-aye's origins has once again called into question the single origins of the lemurs. Comparisons have been made between the Aye-aye and a fossil strepsirrhine primate from Africa, Plesiopithecus. Similarities in the shape of the skull and the morphology of the lower jaw have raised the question of whether or not this could be an Aye-aye ancestor. However, the placement of an Aye-aye ancestor in Africa would require multiple colonizations by strepsirrhine primates. Molecular tests may offer support since they show that the Aye-aye was the first to diverge in the lemur clade and that the other lemur families did not diverge until much later.[5]

Often classified with the galagos by early students, the cheirogaleids were placed with the other lemurs from Gregory's 1915 classification until the early 1970s, when several anthropologists proposed that they are more closely related to lorisiforms, based on morphological data.[68][80] However, relevant genetic studies nearly unanimously place cheirogaleids within the lemuriform clade and Groves, who had promoted the cheirogaleid-lorisiform relationship in a 1974 paper, by 2001 himself regarded the idea as refuted.[15][79][80]

Lemur phylogeny[27][57][81]
Strepsirrhini 
 Lorisiform clade 

Galagidae



Lorisidae



 Lemur clade 

Daubentonia





Lemuridae



Megaladapidae






Lepilemuridae



Cheirogaleidae






Archaeolemuridae




Palaeopropithecidae



Indriidae









Classifications in the first half of the 20th century divided lemurs into three families—Daubentoniidae, Indriidae, and Lemuridae, with the latter including the current Cheirogaleidae and Lepilemuridae.[68] Because of concerns that Lemuridae might not be monophyletic, the family was later split; in 1982, for example, Tattersall separated the Cheirogaleidae for the dwarf lemurs, mouse lemurs, and relatives and the Lepilemuridae for the sportive lemurs and bamboo lemurs (including the Greater Bamboo Lemur).[82] This classification is still used, except that the bamboo lemurs are placed in Lemuridae.[83][61]

From the 1970s to the 1990s, there have been suggestions that the ruffed lemurs might be related to indriids or a sister group to Lemuridae and Indriidae and that the bamboo lemurs are related to the sportive lemurs,[84] but neither view is supported by molecular phylogeny.[27] The sportive lemurs and the extinct koala lemurs (Megaladapidae) both lack upper incisors in the permanent dentition,[73] and in 1981, Groves placed both together in the family Megaladapidae, which he renamed Lepilemuridae in 2005 because that older name takes precedence.[85] Genetic research does not support a close relationship between the sportive and koala lemurs and instead places the koala lemurs as a sister group to Lemuridae; therefore, the two are now placed in separate families (Lepilemuridae for the sportive lemurs and Megaladapidae for the koala lemurs).[86][87][81] The sloth lemurs (Palaeopropithecidae) and monkey lemurs (Archaeopithecidae) were classified as subfamilies within Indriidae as late as 1982,[82] but are now recognized as separate families.[81]

The relationships among the families of lemurs have been problematic and have yet to be definitively resolved. Two competing phylogenies exist based on genetic and molecular data. One approach (Horvath, et al.) looks at a larger number of genes, but among fewer species. This results in Lemuridae being a sister group to Lepilemuridae, Cheirogaleidae, and Indriidae.[27] The other approach (Orlando, et al.) looks at fewer genes, but more lemur species. Using this analysis, Lepilemuridae becomes the sister group to Lemuridae, Cheirogaleidae, and Indriidae.[81] Both phylogenies agree that the Malagasy primates are monophyletic and that Daubentoniidae (the Aye-aye) is basal to the lemuriform clade, having split off significantly earlier than the other families.[15][27][81] However, two problems create complications for both approaches. First, the four most closely related lemur families diverged within a narrow window of approximately 10 million years, making it much harder to distinguish the splits with molecular evidence. Second, the divergence occurred approximately 42 mya;[17] such distant splits create a lot of noise for molecular techniques.

Genus-level classification

Early classifications of the genera of lemurs differed in a number of ways from current taxonomy. For example, the fork-marked lemurs were initially placed in the genus Lemur and then in Microcebus with the mouse lemurs before being placed in their own genus Phaner;[47][88][67][89] and Charles Immanuel Forsyth Major split the Cheirogaleus medius species group of the dwarf lemurs into a separate genus Opolemur, but this was not accepted.[89][67] Genus-level taxonomy was largely stabilized by Schwarz in 1931,[67] but a number of changes have become accepted:

  • The Ring-tailed Lemur, ruffed lemurs, and true lemurs were once grouped together in the genus Lemur due to a host of morphological similarities. For instance, the skeletons of the Ring-tailed Lemur and the true lemurs are nearly indistinguishable.[50] However, ruffed lemurs were reassigned to the genus Varecia in 1962,[90] and due to similarities between the Ring-tailed Lemur and the bamboo lemurs, particularly in regards to molecular evidence and scent glands similarities, the true lemurs were moved to the genus Eulemur in 1988.[49][50][91] The genus Lemur is now monotypic, containing only the Ring-tailed Lemur.
  • In 2001, Colin Groves concluded that despite similarities, the Greater Bamboo Lemur was sufficiently distinct from the bamboo lemurs of the genus Hapalemur to merit its own monotypic genus, Prolemur.[50][92] This follows Schwarz's 1931 opposition to Pocock's decision to separate Prolemur from Hapalemur.[67]
  • Originally placed in the genus Microcebus (mouse lemurs), the Giant Mouse Lemur was moved to its own genus, Mirza, in 1985 due to its larger size, morphological differences, dental characteristics, and behavior.[47][93]
  • The Hairy-eared Dwarf Lemur was first placed in the genus Cheirogaleus (dwarf lemurs) in 1875 and was later found to have closer affinities with Microcebus. However, its dentition and cranium structure were sufficiently distinct to merit elevation to its own genus, Allocebus.[47][94]

Species-level classification

Over the past two decades, the number of recognized lemur species has more than doubled according to some experts. In 1994, 32 distinct species were named in the first edition of Conservation International's field guide, Lemurs of Madagascar, and 68 were described in the 2nd edition, published in 2006.[58][95] In December 2008, Russell Mittermeier, Colin Groves, and other experts co-wrote an article in the International Journal of Primatology classifying 99 species and subspecies.[61] The number of lemur species is likely to continue growing in the coming years, as field studies, cytogenetic and molecular genetic research continues, particularly on cryptic species, such as mouse lemurs, which cannot be distinguished visually.[58]

(Lepilemur sahamalazensis) was identified as a distinct species as recently as 2006.]]

This threefold increase in nearly 15 years has not had universal support among taxonomists and lemur researchers. In many cases, classifications ultimately depends upon which species concept is used. Due to the critical condition that most Malagasy primate populations are in, taxonomists and conservationists sometimes favor splitting them into separate species to develop an effective strategy for the conservation of the full range of lemur diversity.[58][61] Implicitly, this means that full species status will help grant genetically distinct populations added environmental protection.[58]

The first large wave of new lemur species descriptions came in 2001 when Colin Groves elevated the Red Ruffed Lemur (Varecia rubra),[50][96] five subspecies of brown lemur (Eulemur albifrons, E. albocollaris, E. collaris, E. rufus and E. sanfordi),[97] and four subspecies of sifaka (Propithecus coquereli, P. deckenii, P. edwardsi, and P. perrieri) to full species status.[98] Additional elevations of all remaining subspecies within the Eulemur and Propithecus genera were made in the years that followed.[49][50][99] These and subsequent changes in taxonomy were largely due to a shift to the phylogenetic species concept,[100] yet are not universally endorsed.[60]

By far the most explosive growth in species numbers has been in the genera Microcebus and Lepilemur. In 2006, 15 new species of Lepilemur were described, with three new species reported in February,[101] one species in June,[102] and 11 in September.[103] Since then, two additional species have been described.[61] Genetic and morphological differences seem to suggest that they are cryptic species, but there is still debate whether these merit full species status or should be regarded as subspecies of previously identified, "core" species.[60][86]

In true lemurs and mouse lemurs, both groups were initially divided into a small number of species, either with no distinguishable subspecies (in the case of mouse lemurs) or with several distinguishable subspecies (in the case of true lemurs).[10][37] With molecular research suggesting a more distant split in both genera, these subspecies or undistinguished populations have been promoted to species status.[37]

In the case of mouse lemurs, the rise in species numbers has been only slightly less sudden and dramatic. Classified as one species by Ernst Schwarz in 1931 (excluding one, Coquerel's Giant Mouse Lemur, that is no longer classified in Microcebus),[67] the genus was revised to contain two species, the Gray Mouse Lemur (Microcebus murinus) and the Brown Mouse Lemur (M. rufus), after an extensive field study in 1972 showed both living in sympatry in southeastern Madagascar.[104] At the time, the Gray Mouse Lemur was known in the drier parts of the north, west, and south, while the Brown Mouse Lemur inhabited the humid rainforest regions of the east. However, we now know the species diversity and distribution to be significantly more complex.[47] Revisions throughout the 1990s and 2000s identified numerous new species through genetic testing using mitochondrial DNA, demonstrating that the genus is represented by a multitude of cryptic species.[61][105][106][107] Many, but not all of these defined species have been supported by nuclear DNA tests.[108]

However, there are still concerns that species are being identified prematurely. Ian Tattersall, an anthropologist who recognized 42 species of lemur in 1982,[109] has expressed concern that the geographically organized variety in lemur populations is being recognized with full species status while the number of subspecies in lemur genera has virtually disappeared. He has argued that taxonomists are confusing differentiation and speciation, two processes that are often unrelated, while denying the role of microevolution in evolutionary processes.[60] Still, other researchers who emphasize the framework of the "general lineage concept of species" contend that lineage divergence or differentiation demarcates the beginning of a new species.[108]

New species have been identified due to differences in morphology, karyotypes, cytochrome b sequences, and other genetic tests, as well as several combinations of these.[60] When nuclear DNA (nDNA) was tested in conjunction with mitochondrial DNA (mtDNA) in mouse lemurs, a few species, such as Claire's Mouse Lemur (Microcebus mamiratra) were demonstrated to be indistinguishable from other closely related species. In such cases, nDNA did not vary, but the mtDNA that had been used to define it as a species was still distinct. Differences in results between nDNA, which is inherited from both parents, and mtDNA, which is inherited from the mother, was attributed to female philopatry, where females remain within or close to the home range into which they were born while males disperse. Since the isolated population known as Claire's Mouse Lemur has distinct mtDNA, but not nDNA, it is likely to contain a population descended from a related group of females, but which still disperses and interbreeds with nearby populations.[108]

Traditionally, karyology has been considered when determining species status. From the lemurs studied so far, the diploid number of chromosomes in lemurs varies between 2n=20 and 2n=66. In the case of the true lemurs, the diploid number ranges from 2n=48 to 2n=60 while the individual chromosome sizes vary considerably.[77]

Sometimes distinctions are made due to very slight differences in pelage coloration. For instance, three distinctly-colored types of mouse lemur were discovered in a multi-year study in Beza Mahafaly Reserve in southern Madagascar, but rather than being separate species, DNA tests revealed that they all belonged to a single species, the Reddish-gray Mouse Lemur (Microcebus griseorufus).[110] For this reason, further research is needed to confirm or deny the recent species splits. Only through detailed studies of morphology, ecology, behavior, and genetics can the true number of lemur species be determined.[58]

Lemur species and subspecies count by year and genus
1931
Schwarz[67]
1982
Tattersall[109]
1994
Mittermeier et al.[111]
2005
Groves[83]
2006
Mittermeier et al.[95]
2010
Mittermeier et al.[112]
genus species subspecies species subspecies species subspecies species subspecies species subspecies species subspecies
Allocebus[N 2] 1 0 1 0 1 0 1 0 1 0
Avahi 1 2 1 2 2 0 3 0 4 0 9 0
Cheirogaleus[N 2] 3 4 2 0 2 0 7 0 7 0 5 0
Daubentonia 1 0 1 0 1 0 1 0 1 0 1 0
Eulemur[N 3] 5 8 11 2 10 2 12 0
Hapalemur[N 4] 2 2 2 3 3 3 4 2 5 0 5 3
Indri 1 0 1 0 1 0 1 2 1 0 1 0
Lemur[N 3][N 5] 6 7 4 7 1 0 1 0 1 0 1 0
Lepilemur 2 0 1 6 7 0 8 0 8 0 26 0
Microcebus[N 6] 2 2 2 0 3 0 8 0 12 0 18 0
Mirza[N 6] 1 0 1 0 1 0 2 0 2 0
Phaner 1 0 1 0 1 4 4 0 4 0 4 0
Prolemur[N 4] 1 0 1 0 1 0
Propithecus 2 9 2 9 3 8 7 4 9 0 9 0
Varecia[N 5] 1 2 1 2 1 4 2 3 2 3
Totals[N 7] 21 26 20 29 32 25 59 14 68 5 97 6
38 42 50 67 71 101

Notes

  1. ^ Propithecus diadema holomelas was once considered one of five subspecies of Diademed Sifaka. In 1986, Ian Tattersall subsumed it as a synonym for what is now known as Milne-Edwards' Sifaka (known then as Propithecus diadema edwardsi). Both subspecies had only slight color variations and were known to be sympatric with each other in at least one forest.[52] Since it was extirpated, the taxonomic status of Propithecus diadema holomelas has been questioned, but nothing definitive has been published.[53]
  2. ^ a b In 1931, Allocebus was not recognized as a separate genus, but was lumped under the genus Cheirogaleus.
  3. ^ a b In 1931 and 1982, Eulemur was not recognized as a separate genus, but was lumped under the genus Lemur.
  4. ^ a b The genus Prolemur was not distinguished until 2001. Prior to this, the Greater Bamboo Lemur was placed in the genus Hapalemur.
  5. ^ a b In 1931, Varecia was not recognized as a separate genus, but was lumped under the genus Lemur.
  6. ^ a b In 1931, Mirza was not recognized as a separate genus, but was lumped under Microcebus.
  7. ^ The grand total of species and subspecies for each year will not equal the sum of the species total and the subspecies total since each subspecies group already counts as one species. For example, in 2010 there were three subspecies for Varecia variegata recognized: V. v. variegata, V. v. editorum, and V. v. subcincta. Together, they count as one species, which is already included in the species total for that year. The same applies that year for Hapalemur. For this reason there are 101 species and subspecies (97 − 2 + 6 = 101), not 103. In 1994, there were seven species with subspecies listed, so the grand total is: 32 − 7 + 25 = 50

References

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Books cited
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Chapter 2 - Geology and Soils
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  • Krause, D.W. (2003). "Late Cretaceous Vertebrates of Madagascar: A Window into Gondwanan Biogeography at the End of the Age of Dinosaurs". pp. 40–47. 
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Chapter 13 - Mammals
  • Goodman, S.M.; Ganzhorn, J.U.; Rakotondravony, D. (2003). "Introduction to the Mammals". pp. 1159–1186. 
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