Lemurs are 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. Primates first evolved sometime between the
Middle Cretaceous and the early
Paleocene periods on either the
supercontinent of
Laurasia or in Africa. According to
molecular clock studies, the last common ancestor of all primates dates to around 79.6 mya, although the earliest known
fossil primates are only 54–55 million years old. The closest relatives of primates are the extinct
plesiadapiforms, the modern
colugos (commonly and inaccurately named "flying lemurs"), and
treeshrews. 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
haplorhines (
tarsiers,
monkeys,
apes, and
humans) and strepsirrhines is 58 to 63 mya. A consensus is emerging that places omomyids as a
sister group to tarsiers, eosimiids as a
stem group to
simians (non-tarsier haplorhines), and
Djebelemur, an African genus likely to be related to an early Asian branch of
cercamoniine adapiforms, as a stem group to modern strepsirrhines, including lemurs. 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. Media sources inaccurately dubbed the fossil as a "missing link" between lemurs and humans. , a trait shared by lemurs with their closest relatives, the
lorisoids, provides insight into both the evolutionary history of strepsirrhines and the lemur colonization of Madagascar. Lemurs were traditionally thought to have evolved during the
Eocene (55 to 37 mya) based on the fossil record, although molecular tests suggest the Paleocene (66 to 56 mya) or later. Until recently, they were thought to have descended directly from the diverse group of adapiforms due to several shared
postcranial traits, as well as long
snouts and small
brains. Although adapiforms also had lemur-like
auditory bullae, a prosimian characteristic, they had smaller brains and longer snouts than lemurs. There are also several other
morphological differences. Most noticeably, adapiforms lack a key
derived trait, the
toothcomb, and possibly the
toilet-claw, found not only in
extant (living) 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. Comparative studies of the
cytochrome b gene, which are frequently used to determine phylogenetic relationships among mammals—particularly within families and genera—have been used to show that lemurs share common ancestry with lorisoids. This conclusion is also corroborated by the shared strepsirrhine toothcomb, an unusual trait that is unlikely to have evolved twice. If adapiforms were the ancestors of the living strepsirrhines, then the last common ancestor of modern strepsirrhines would have to predate the early Eocene, a view supported by
molecular phylogenetic studies by
Anne D. Yoder and Ziheng Yang in 2004, which showed that lemurs split from lorises approximately 62 to 65 mya. These dates were confirmed by more extensive tests by Julie Horvath
et al. in 2008. These molecular studies also showed that lemuroids diversified before the modern lorisoids. Using a more limited data set and only
nuclear genes, another study in 2005 by Céline Poux
et al. 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. However, the 2003 discovery of fossil lorisoids at the
Fayum Depression in Egypt pushed the date of lorisoid divergence back to the Eocene, matching the divergence dates predicted by Yoder and Horvath. The
fossil record tells a different story. Although it cannot 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 66 million years, then the first one-third of the primate fossil record is missing. Another problem is that some of these molecular dates have overestimated the divergence of other mammalian orders, such as
Rodentia, suggesting primate divergence might also be overestimated. One of the oldest known strepsirrhines,
Djebelemur, dates from the early Eocene of 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. To complicate the ancestry puzzle, no terrestrial Eocene or Paleocene
fossils have been found on Madagascar, and the fossil record from both Africa and Asia around this time is not much better. Fossil sites in Madagascar are restricted to only five windows in time, which omit most of the
Cenozoic, from 66 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. The oldest lemur fossils on Madagascar are actually
subfossils dating to the
Late Pleistocene.
Colonization of Madagascar Once part of the supercontinent
Gondwana, Madagascar broke away from eastern Africa, the most 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, a deep channel with a minimum width of approximately . These separation dates and the estimated age of the primate lineage preclude any possibility that lemurs could have been on the island before Madagascar pulled away from Africa, an evolutionary process known as
vicariance. 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. 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. By the early 20th century,
oceanic dispersal emerged as the most popular explanation for how lemurs reached the island. 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". In the 1940s, American paleontologist
George Gaylord Simpson coined the term "sweepstakes dispersal" for such unlikely events. As plate tectonics theory took hold, oceanic dispersal fell out of favor and was even considered by many researchers to be "miraculous" if it occurred. Despite the low likelihood of its occurrence, oceanic dispersal remains the most accepted explanation for numerous vertebrate colonizations of Madagascar, including that of the lemurs. 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. Any extended ocean voyage without fresh water or food would prove difficult for a large,
warm-blooded (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. However, this trait has not been observed in the closely related lorisoids studied to date, and could have evolved on Madagascar in response to the island's harsh environmental conditions. Because only five terrestrial
orders of mammals have made it to the island, each likely to have derived from a single colonization, 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. A report published in January 2010 supported this assumption by demonstrating that both Madagascar and Africa were 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. 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, is that
stem strepsirrhines evolved on the Afro-Arabian landmass, dispersing to Madagascar and more recently from Africa to Asia. 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. 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. However, this is unlikely since the only seamounts found along the
Davie Ridge would have been too small in such a wide channel. Even though the
Comoro Islands between Africa and Madagascar are significantly larger, they are too young, having been formed by volcanic activity only around 8 mya. 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. A variant of the land bridge hypothesis has been proposed in an attempt to explain both how a land bridge could have formed, and why other mammalian orders failed to cross it. 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, or possibly as early as 55 mya. 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. The divergence dates of many Malagasy mammalian orders formerly fell within this window.
Old World monkeys, dogs, and cats did not diverge or arrive in Africa until later in the Miocene. However, 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. The dating of the lemur colonization is controversial for the same reasons as strepsirrhine evolution. Using both mitochondrial and nuclear DNA sequences, a single colonization has been estimated at 62 to 65 mya based on the split between the
aye-aye and the rest of the lemurs. On the other hand, the sparse fossil record and some estimates based on other nuclear genes support a more recent estimate of 40 to 52 mya. Furthermore, a fossil strepsirrhine primate from Africa,
Plesiopithecus, may suggest that the aye-aye and the rest of the lemurs diverged in Africa, which would require at least two colonization events. Once safely established on Madagascar, with its limited mammalian population, the lemurs were protected from the increasing competition from evolving
arboreal mammalian groups.
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 and leaving only the
nocturnal lorisoids.
Diversification }} |1=Daubentoniidae |2= }} }} }} The ancestral lemur that colonized Madagascar is thought to have been small and nocturnal. 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. Nothing definitive is known about the island's
biogeography at the time of the colonization, however, the
paleoclimate (ancient weather patterns) may have been affected by Madagascar's location below the
subtropical ridge at 30° S latitude and disruption of the weather patterns by India as it drifted northward. Both would have created a drying effect on Madagascar, and as a result, the
arid spiny bush that is currently found in the south and southwest of Madagascar would have dominated the island. This would have placed strong
selection pressure for
drought tolerance on the inhabitants of the island between the Cretaceous and the Eocene. As Madagascar edged above the subtropical ridge and India moved closer to Asia, the climate became less dry and the arid spiny bush retreated to the south and southwest. Lemurs have diversified greatly since first reaching Madagascar. The aye-aye and its extinct relations are thought to have diverged first, shortly after colonization. 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 in the first diversification episode, during a 10 to 12 million-year window between the Late Eocene (42 mya) and into the Oligocene (30 mya). The dates for this divergence window span the
Eocene–Oligocene extinction event, during which time climate cooling took place and changes in ocean currents altered weather patterns. Outside of Madagascar, these dates also coincide with the divergence of the lorisoid primates and five major clades of squirrels, all occupying niches similar to those of lemurs. 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. The precise relationship between the four of the five families of lemurs is disputed since they diverged during this narrow and distant window. Although all studies place Cheirogaleidae and Lepilemuridae as a sister clade to Indriidae and Lemuridae, some suggest that Cheirogaleidae and Lepilemuridae diverged first, while others suggest that Indriidae and Lemuridae were the first to branch off. 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). This event coincided with the beginning of the Indian
monsoons, the last major change in climate to affect Madagascar. The populations of both the true lemurs and mouse lemurs were thought to have diverged due to
habitat fragmentation when humans arrived on the island roughly 2,000 years ago. Only recently has molecular research shown a more distant split in these genera. 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. Studies in
karyology, molecular genetics, and
biogeographic patterns have also assisted in understanding their phylogeny and diversification. Although the divergence estimates for these two genera are imprecise, they overlap with a change to a wetter climate in Madagascar, as new weather patterns generated
monsoons and likely influenced the plant life. This difference in evolutionary divergence between the two genera may be due to differences in their activity patterns. True lemurs are often
diurnal, allowing potential mates 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. ==Distribution and diversity==