Lemur hybrids

Family Lemuridae

Mammalian Hybrids

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EUGENE M. MCCARTHY, PHD GENETICS, ΦΒΚ

     
Varecia variegata Black-and-white Ruffed Lemur
Varecia variegata

Varecia rubra Red Ruffed Lemur
Varecia rubra

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Note: Several of the following taxa (albifrons, albocollaris, cinereiceps, collaris, fulvus, rufiventer, rufus, sanfordi) have often been treated as subspecies of Eulemur fulvus.

Note: Albignac et al. (1971) give physical descriptions of the various Eulemur hybrids cited below.

Eulemur albifrons [White-fronted Lemur]
× Eulemur fulvus (♂) [Brown Lemur] CHR. HPF(♂&♀). CON: western Madagascar (inland from Toamasia, Maningory River). Since Albignac et al. (1971) mention a male hybrid that sired an offspring, female hybrids, too, may be presumed partially fertile (by Haldane’s Rule). These taxa are sometimes lumped. Egozcue 1967; International Zoo Yearbook 1967 (p. 302), 1972 (p. 315); Rumpler 1975; Schwarz 1931.
× Eulemur macaco (↔) [Black Lemur] CHR. CON: northern Madagascar? Albignac et al. 1971; International Zoo Yearbook 1971 (p. 262), 1974 (p. 367); Rumpler 1975; von Knottnerus-Meyer 1904.
× Eulemur mongoz [Mongoose Lemur] CHR?? DRS. von Knottnerus-Meyer 1904.

Note. Here, albocollaris is treated as a synonym of cinereiceps (see Johnson et al. 2008), but albocollaris is the name used in most of the reports of hybrid crosses listed here as involving cinereiceps.

Eulemur cinereiceps [White-collared Lemur]
× Eulemur collaris [Red-collared Lemur] CHR. CON: southeastern Madagascar. LFH. These taxa are sometimes lumped. Djlelati et al. 1997; Rumpler and Albignac 1975.
× Eulemur fulvus [Brown Lemur] CHR. HPF(♀♀). DRS. These lemurs produce partially fertile hybrids despite a large difference in their chromosome count (E. cinereiceps: 2n = 48; E. fulvus: 2n = 60). A partially fertile female three-way hybrid with an E. macaco male has been produced. These taxa are sometimes lumped. Djlelati et al. 1997; Rumpler 1975; Rumpler and Albignac 1975.
× Eulemur rufifrons [Red-fronted Lemur] CAENHR(southeastern Madagascar). HPF(♂&♀). A 60-kilometer-wide hybrid zone exists at the Iantara River (headwaters of the Manampatrana) southeast of the Andringitra Massif. About 58 hybrids occur there per km² (Irwin et al. 2005; Wyner et al. 2002). Testicular biopsy indicates that male hybrids are about as fertile as pure parental males. Wyner et al. (p. 63) say some alleles were unique to the hybrid population. Rumpler reports a three-way cross with E. fulvus. These taxa are sometimes lumped. Dutrillaux and Rumpler 1997; Goodman and Ganzhorn 2004; Johnson 2002; Johnson and Wyner 2000; Pastorini et al. 2009; Ratomponirina et al. 1982; Rumpler 1975; Sterling and Ramarason 1996; Wyner et al. 2002.
× Eulemur macaco [Black Lemur] CHR. DRS. LFH. Djlelati et al. 1997; Ratomponirina et al. 1988; Rumpler 1975, 2004; Rumpler and Dutrillaux 1976.

Eulemur collaris [Red-collared Lemur]
See also: Eulemur cinereiceps.
× Eulemur fulvus (♀) [Brown Lemur] CHR. DRS. HPF. These taxa are sometimes lumped. Djlelati et al. 1997; Hill 1953 (p. 311); Rumpler 1975; Rumpler and Albignac 1975.
× Eulemur macaco (♂)[Black Lemur] CHR. DRS. Hybrids of both sexes have been reported. Spermatogenesis is severely disrupted in hybrids (spermatids and spermatozoa are rare). Chromosomes form elongated chains during meiosis. Albignac et al. 1971; International Zoo Yearbook 1971 (p. 262), 1974 (p. 367); Ratomponirina et al. 1982; Rumpler 1975.
× Eulemur mongoz [Mongoose Lemur] CHR. DRS. Citing Sclater (1863), Przibram (1910, p. 111) lists the cross Lemur nigrifrons (= E. mongoz) × L. xanthomystax (= E. collaris). Rumpler and Dutrillaux 1976.
× Eulemur rufifrons (♂) [Red-fronted Lemur] CHR. DRS. HPF(♂&♀). The IUCN (Internet Citations: RUCOL) says a small group of hybrids of this type is present in the Berenty Private Reserve in southern Madagascar. F₂ hybrids have been reported (International Zoo Yearbook 1974). These taxa are sometimes lumped. Albignac et al. 1971; International Zoo Yearbook 1972 (p. 315), 1974 (p. 367); Moses et al. 1979.

Eulemur coronatus [Crowned Lemur]
× Eulemur macaco (♀) [Black Lemur] CHR. CON: broad overlap northwestern Madagascar. LFH. A female hybrid had the shiny red pelage of an E. macaco female, but the top of the head was darker and the tail like that of E. coronatus. There were lateral white head tufts, but less developed than in E. macaco. The muzzle resembled E. macaco, the ears, those of E. coronatus, but with darker fur. De Boer 1973; Djlelati et al. 1997; Ratomponirina et al. 1988; Warter and Rumpler 1985.
× Eulemur mongoz [Mongoose Lemur] Parapatric contact zone (northwestern Madagascar, lower Betsiboka). These lemurs are sometimes lumped, but no hybrids are as yet reported. Hill 1953 (Fig. 137 and p. 425); Ronchetti et al. 1997.

Eulemur flavifrons [Blue-Eyed Black Lemur]
× Eulemur macaco [Black Lemur] ENHR. CON: northern Madagascar. Rabarivola et al. state that "A study of intermediate forms between Eulemur macaco macaco and E. m. flavifrons was performed on animals in different areas located to the north, south, and east of the known limits of distribution in Maromandia. A large hybridization zone was defined and morphological and dermatoglyphic comparisons were done on the different animals." These taxa have often been lumped due to hybridization, but are currently treated separately by the IUCN despite the occurrence of extensive hybridization (http://www.iucnredlist.org/details/full/8211/0; accessed Dec. 2013). These two lemurs are markedly different in coloration. Rabarivola et al. 1991.

Eulemur fulvus [Brown Lemur]
See also: Eulemur albifrons; E. cinereiceps; E. cinereiceps ×E. collaris;E. collaris.
× Eulemur macaco (↔)[Black Lemur] CHR. HPF(♀♀). These hybrids were formerly common in captivity. CON: northern Madagascar. A captive hybrid lived 39 years. Albignac et al. 1971; Ashley Montagu 1950; Hamilton and Moses 1979; Hill 1953 (p. 311); International Zoo Yearbook 1960 (p. 255), 1971 (p. 262), 1974 (p. 367); Moog 1959; Ratomponirina et al. 1982; Rumpler 1975; Rumpler and Dutrillaux 1976, 1980; Zuckerman 1932 (p. 1069), 1953 (p. 943). Internet Citations: DEMO.
× Eulemur mongoz (↔) [Mongoose Lemur] ENHR(northern Madagascar). Zaramody and Pastorini 2001; Zuckerman 1932 (p. 1069), 1953 (p. 943). Internet Citations: EULEM.
× Eulemur rubriventer (♀) [Red-bellied Lemur] CHR. CON: eastern Madagascar (between Antananarivo and the west coast). Ratomponirina et al. say germ cells were absent in three male hybrids. A male hybrid described by Saint-Pie was very similar to its dam (E. rubriventer), but had a cross on its forehead recalling E. fulvus. Albignac et al. 1971; (p. 365); International Zoo Yearbook 1970 (p. 251), 1971 (p. 262), 1972 (p. 315), 1978 (p. 370); Ratomponirina et al. 1982; Rumpler and Dutrillaux 1980; Saint-Pie 1970.
× Eulemur rufifrons (↔) [Red-fronted Lemur] CAENHR(eastern Madagascar). HPF(♀♀). CON: in the vicinity of Marolambo. These taxa are sometimes lumped. Albignac et al. 1971; Glander and Rabin 1983; Goodman and Ganzhorn 2004; Hill 1953 (pp. 415, 417); International Zoo Yearbook 1967 (p. 302), 1971 (p. 262), 1972 (p. 315) 1979 (p. 349); Lehman and Wright 2000; Pastorini et al. 2009; Rumpler 1975; Sheine and Kay 1981; Zuckerman 1953 (p. 943). Internet Citations: LEMUR.
× Eulemur sanfordi (♀) [Sanford’s Lemur] CHR. DRS. Albignac et al. 1971; Rumpler 1975.
× Eulemur rufifrons [Red-fronted Lemur] ENHR. CON: in the vicinity of Marolambo, Madagascar. Lehman and Wright 2000.

Eulemur macaco [Black Lemur]
See also: Eulemur albifrons; E. cinereiceps; E. collaris; E. coronatus; E. flavifrons; E. fulvus.
× Eulemur mongoz (↔) [Mongoose Lemur] CHR. Probable parapatric contact zone in northwestern Madagascar, lower Betsiboka. A hybrid lived four days. Ashley Montagu 1950; Chiarelli 1961; Zuckerman 1953 (p. 943).
× Eulemur rufifrons (↔) [Red-fronted Lemur] CAENHR. CON: northwestern Madagascar, lower Betsiboka. In the case of a hybrid (male E. macaco ×female E. rufifrons) exhibited at the Zoological Society of London Pocock (p. 5) noted that “the offspring resembled neither of its parents. It had not inherited the facial fringe of its father nor the white over the eyes and on the forehead of its mother, this area of the head being dark ashy black with a deeper tinted central line, more approaching the colour seen in the Black-fronted variety of the Fulvous Lemur.” Albignac et al. 1971; International Zoo Yearbook 1971 (p. 262), 1974 (p. 367); Pocock 1911a; Rumpler and Albignac 1969.

Eulemur mongoz [Mongoose Lemur]
See: Eulemur albifrons; E. collaris; E. fulvus; E. macaco.
× Eulemur rufifrons [Red-fronted Lemur] ENHR. HPF. CON: west Madagascar. Pastorini et al. (2009) confirmed the hybrid status of eight individuals from the vicinity of Anjamena. In their abstract, these authors state that "Two segments of mtDNA have been sequenced and 12 microsatellite loci screened in 162 brown lemurs and mongoose lemurs. Among the mongoose lemur population at Anjamena, we identified two F₁ hybrids (one also having the mtDNA haplotype of E. fulvus) and six other individuals with putative introgressed alleles in their genotype. Principal component analysis groups both hybrids as intermediate between E. mongoz and E.Fred fulvus and admixture analyses revealed an admixed genotype for both animals. Paternity testing proved one F₁ hybrid to be fertile. Of the eight brown lemurs genotyped, all have either putative introgressed microsatellite alleles and/or the mtDNA haplotype of E. mongoz." Photo of a hybrid.

Eulemur rubriventer [Red-bellied Lemur]
See also: Eulemur fulvus.
× Eulemur rufifrons[Red-fronted Lemur] CHR. BRO: west central Madagascar. Woodburn Safari Park, UK, had a hybrid of this type in 2014.

Eulemur rufifrons [Red-fronted Lemur] See: Eulemur cinereiceps; E. collaris; E. fulvus; E. macaco; E. mongoz; E. rubriventer Here, rufifrons is treated as a synonym of Eulemur rufus. In the Mania River valley on the west coast of Madagacar, rufus and rufifrons come into parapatric contact and may hybridize. Some crosses listed here as involving rufifrons may instead have involved rufus.

Eulemur rufus [Red Brown Lemur] See: Eulemur rufifrons.

Eulemur sanfordi [Sanford’s Lemur] See: Eulemur fulvus.

Hapalemur griseus [Grey Bamboo Lemur]
× Hapalemur alaotrensis [Alaotran Bamboo Lemur] CHR. CON: vicinity of Lake Alaotra, northeastern Madagascar. Rumpler 1975.
× Hapalemur meridionalis [Southern Lesser Bamboo Lemur] ENHR(southern Madagascar). An animal from Atsimo was a hybrid of this type (Rabarivola et al. 2007). The IUCN Red List (http://www.iucnredlist.org/details/136384/0 accessed 12/30/2013) says "animals from 1,600 m on the Andringitra Massif are now either H. meridionalis or hybrids between H. griseus and H. meridionalis)." See also: Warter and Tattersall 1994.
× Hapalemur occidentalis [Sambirano Lesser Bamboo Lemur] CHR. Parapatric contact in northeastern Madagascar. Rumpler 1975.
× Prolemur simus [Greater Bamboo Lemur] CHR(Parc Zoologique de Paris). CON: southeastern Madagascar (humid forest, east of Fianaratsoa). Internet Citations: LESZ.

Hapalemur alaotrensis [Alaotran Bamboo Lemur] Listed as critically endangered by the IUCN. See: Hapalemur griseus.

Hapalemur meridionalis [Southern Lesser Bamboo Lemur] Listed as vulnerable by the IUCN. See: Hapalemur griseus.

Hapalemur occidentalis [Sambirano Lesser Bamboo Lemur] Listed as vulnerable by the IUCN. See: Hapalemur griseus.

Lepilemur mustelinus [Weasel Sportive Lemur]
× Lepilemur ruficaudatus [Red-tailed Sportive Lemur] Parapatric contact zone (extreme southwestern Madagascar, near Andrahomana). No hybrids as yet reported. Hill 1953 (Fig. 148).

Lepilemur ruficaudatus [Red-tailed Sportive Lemur] See: Lepilemur mustelinus.

Lepilemur septentrionalis [Northern Sportive Lemur] Ravaoarimanana et al. (1999) state that "Lepilemur septentrionalis includes four subspecies characterized by different karyotypes: one with 34 chromosomes, two with 36 chromosomes, and one with 38 chromosomes (Petter et al. 1977). Numerous fertile natural hybrids with 35 and 37 chromosomes occurred indicating the absence of reproductive barriers between these subspecies."

Prolemur simus [Greater Bamboo Gentle Lemur] See: Hapalemur griseus.

Varecia rubra [Red Ruffed Lemur]
× Varecia variegata (♀) [Black-and-white Ruffed Lemur] CANHR(northern Madagascar). The hybrids are at least partially fertile. Vasey and Tattersall provide an excellent summary of evidence for hybridization, both natural and in captivity. They (p. 16) note that these rather different-looking lemurs were lumped on the basis of hybrid specimens produced in captivity, which were formerly common. The poorly studied contact zone is in the Maroantsetra region (north of the Bay of Antongil). Several natural hybrids are known. They are black capped and bellied, but vary in the extent of the dark fur on their backs. Light areas vary individually from rufous to light pink. According to the ZooChat website, hybrids produced by backcrossing to a Varecia rubra male are often hairless. Buettner-Janusch and Tattersall 1985; Hill 1953 (p. 401); International Zoo Yearbook 1986 (p. 472), 1988 (p. 450), 1989 (p. 312); Petter 1969; Schwarz 1931; Tattersall 1982; Vasey and Tattersall 2002; Zoological Society of London Annual Report 1972 (p. 12). More information

Varecia variegata [Black-and-white Ruffed Lemur] See: Varecia rubra.

dog-cow hybrid A dog-cow hybrid?

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By the same author: Handbook of Avian Hybrids of the World, Oxford University Press (2006).


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