Evolution of lemurs

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A mouse lemur perched vertically, up-side-down on a branch, looking down at camera.
Mouse lemurs, the smallest primates in the world, evolved in isolation along with other lemurs on the island of Madagascar.

Lemurs, primates belonging to the suborder Strepsirrhini which branched off from other primates less than 63 million years ago, evolved on the island of Madagascar, for at least 40 million years. 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

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, lemurs are now restricted to 10% of the island, or approximately 60,000 square kilometers (23,000 square miles), with many facing extinction.

Evolutionary history

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.[1]

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 million years 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.[5]

The relationship between known fossil primate families remains unclear. A conservative estimate for the divergence of

transitional form between the prosimian and simian lineages.[10] Media sources inaccurately dubbed the fossil as a "missing link" between lemurs and humans.[11]

Close-up of the front, bottom teeth of a ring-tailed lemur, showing the first six teeth pointing directly forward instead of up-and-down like the canine-like premolar behind them.
Fossil evidence for the evolution of the toothcomb, 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

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.[17]

Comparative studies of the

Fayum Depression in Egypt pushed the date of lorisoid divergence back to the Eocene, matching the divergence dates predicted by Yoder and Horvath.[21][22][24]

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.[12]

To complicate the ancestry puzzle, no terrestrial Eocene or Paleocene

subfossils dating to the Late Pleistocene.[14]

Colonization of Madagascar

Once part of the supercontinent

endemic mammals present on the island today.[17]

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

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".[34] In the 1940s, American paleontologist George Gaylord Simpson coined the term "sweepstakes dispersal" for such unlikely events.[35]

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.[30] 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.[30][35] 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.[17][34][36]

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.[36] 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.[17]

Because only five terrestrial orders of mammals have made it to the island, each likely to have derived from a single colonization,[30][31] 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.[17] 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.[37]

Since the 1970s, the rafting hypothesis has been called into question by claims that lemur family

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,[17] is that stem strepsirrhines evolved on the Afro-Arabian landmass, dispersing to Madagascar and more recently from Africa to Asia.[24] 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.[12]

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.[16][27] 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.[27] 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.[38]

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.[12] 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,[39] or possibly as early as 55 mya.[12] 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.[39] 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.[23]

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.[21] 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.[12] 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.[12][40]

Once safely established on Madagascar, with its limited mammalian population, the lemurs were protected from the increasing competition from evolving arboreal mammalian groups.[25] 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.[16][41]

Diversification

Competing lemur phylogenies
Lemuroidea
 
Lemuroidea 

Daubentoniidae

Lepilemuridae

Cheirogaleidae

Lemuridae

†

Megaladapidae

There are two competing lemur phylogenies, one by Horvath et al. (top)[42] and one by Orlando et al. (bottom).[43] Note that Horvath et al. did not attempt to place the subfossil lemurs.

The ancestral lemur that colonized Madagascar is thought to have been small and nocturnal.

cranial foramina and the middle ear—comparable to that of lemurids, while being similar to cheirogaleids in dentition and postcranial anatomy.[12]

Nothing definitive is known about the island's

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.[45] 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.[30][45]

Lemurs have diversified greatly since first reaching Madagascar. The aye-aye and its extinct relations are thought to have diverged first, shortly after colonization.

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).[21][22] 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.[21][12] 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.[21] 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.[44] 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,[43][46] while others suggest that Indriidae and Lemuridae were the first to branch off.[42]

The second major episode of diversification occurred during the Late Miocene, approximately 8 to 12 mya, and included the

sexual dichromatism.[21] Studies in karyology, molecular genetics, and biogeographic patterns have also assisted in understanding their phylogeny and diversification.[47] 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.[21][22]

This difference in evolutionary divergence between the two genera may be due to differences in their activity patterns. True lemurs are often

sexual dichromatism while mouse lemurs evolved to be cryptic species.[21]

Distribution and diversity

See also: Subfossil lemur
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.

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

niche differentiation in sympatry, occasionally hybridization can occur.[41] 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.[14]

Most of the 99 living lemur taxa are found only on Madagascar. Two species, the

endemic
.

Historically, lemurs ranged across the entire island inhabiting a

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.[53] Today, the level of floral diversity increases with precipitation, from the dry southern forests to the wetter northern forests to the rainforests along the east coast. Increased foliage corresponds to increased faunal diversity, including the diversity and complexity of lemur communities.[14]

A giant lemur, Palaeopropithecus ingens, hangs upside down by its long arms and legs, suspended from a branch by curved digits on its hands and feet.
A life restoration of Palaeopropithecus ingens, a giant sloth lemur that became extinct less than a thousand years ago

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,

cathemerality (activity both day and night), and/or strict breeding seasons.[13][54] 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.[55]

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.

subfossil remains, but today it remains one of the world's 25 most endangered primates.[58][59][60][61] One distinctive morph (possibly a species or subspecies) of sifaka,[N 1] has not been so fortunate, having been extirpated from all known localities.[64] Unless trends change, extinctions are likely to continue.[65]

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 evolved in isolation. Some of their adaptations were unlike those seen in lemurs today.[25] All 17 extinct lemurs were larger than the extant forms, some weighing as much as 200 kg (440 lb),[41] and are thought to have been active during the day.[66] 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.[25] 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.[67]

Notes

  1. 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.[62] Since it was extirpated, the taxonomic status of Propithecus diadema holomelas has been questioned, but nothing definitive has been published.[63]

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  2. ^ Bloch et al. 2007, pp. 1159–1164.
  3. ^ a b Janečka et al. 2007, pp. 792–794.
  4. ^ Tavaré et al. 2002, pp. 726–729.
  5. ^ Williams, Kay & Kirk 2010, pp. 4797–4804.
  6. ^ Godinot 2006, p. 459.
  7. ^ Williams, Kay & Kirk 2010, p. 4797.
  8. ^ Williams, Kay & Kirk 2010, p. 4799.
  9. ^ Godinot 2006, pp. 452–453.
  10. ^ Franzen et al. 2009.
  11. ^ Handwerk, B. (19 May 2009). ""Missing link" found: New fossil links humans, lemurs?". National Geographic News. Archived from the original on May 21, 2009. Retrieved 12 September 2009.
  12. ^ a b c d e f g h i Godinot 2006, pp. 446–464.
  13. ^ a b c d Gould & Sauther 2006, pp. vii–xiii.
  14. ^ a b c d e Sussman 2003, pp. 149–229.
  15. ^ Ankel-Simons 2007, pp. 392–514.
  16. ^ a b c d Preston-Mafham 1991, pp. 141–188.
  17. ^ a b c d e f g h i j k Tattersall 2006, pp. 3–18.
  18. ^ Castresana 2001, pp. 465–471.
  19. ^ Yoder 2003, pp. 1242–1247.
  20. ^ Simons 1997, pp. 142–166.
  21. ^ a b c d e f g h i j k Yoder & Yang 2004, pp. 757–773.
  22. ^ a b c d e f Horvath et al. 2008, pp. 488–499.
  23. ^ a b Poux et al. 2005, pp. 719–730.
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  26. ^ Samonds et al. 2009, pp. 1233–1243.
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  33. ^ de Camp 1954, p. 52.
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  41. ^ a b c d Garbutt 2007, pp. 85–86.
  42. ^ a b Horvath et al. 2008, fig. 1.
  43. ^ a b Orlando et al. 2008, fig. 1.
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  47. ^ a b Johnson 2006, pp. 187–210.
  48. ^ a b Mittermeier et al. 2006, pp. 89–182.
  49. ^ a b Mittermeier et al. 2006, pp. 37–51.
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  55. ^ Dunham & Rudolf 2009, pp. 1376–1386.
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  58. ^ a b Mutschler & Tan 2003, pp. 1324–1329.
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  61. ^ Mittermeier et al. 2007, pp. 1–40.
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  67. ^ Godfrey & Jungers 2003, pp. 1247–1252.

Literature cited
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