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Lemur Origins: Rafting by Groups of Hibernators?

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Abstract

When and how non-human primates first arrived on Madagascar remains one of the most enigmatic questions in primate evolution [1-3]. Madagascar broke away from the African mainland and India long before the estimated origin of the first primates [4-7]. Because African and Asian lorises are the closest living relatives of Malagasy primates, however, some of their common ancestors must have migrated to distant islands or continents. Recent phylogenetic analyses strongly indicate an African origin for lemurs and lorises, thereby supporting a primate colonisation of Madagascar from Africa [8], but proposed mechanisms for this transoceanic colonisation have been highly controversial. Here I cite evidence from several recent studies that suggest a likely mechanism for a successful colonisation across the formidable water barrier of the Mozambique Channel.
Brief Report
Folia Primatol 2000;71:422–425
Lemur Origins: Rafting by Groups of
Hibernators?
Peter M. Kappeler
Abteilung Verhaltensforschung/Ökologie, Deutsches Primatenzentrum,
Göttingen, Deutschland
Received: February 9, 2000
Accepted after revision: May 23, 2000
Peter M. Kappeler
Abteilung Verhaltensforschung/Ökologie
Deutsches Primatenzentrum, Kellnerweg 4
D–37077 Göttingen (Germany)
E-Mail pkappel@gwdg.de
ABC
Fax + 41 61 306 12 34
E-Mail karger@karger.ch
www.karger.com
© 2001 S. Karger AG, Basel
0015–5713/00/0716–0422$17.50/0
Accessible online at:
www.karger.com/journals/fpr
Key Words
Primate evolution
W Lemurs W Madagascar W Biogeography
Introduction
When and how non-human primates first arrived on Madagascar remains one of
the most enigmatic questions in primate evolution [1–3]. Madagascar broke away from
the African mainland and India long before the estimated origin of the first primates
[4–7]. Because African and Asian lorises are the closest living relatives of Malagasy
primates, however, some of their common ancestors must have migrated to distant
islands or continents. Recent phylogenetic analyses strongly indicate an African origin
for lemurs and lorises, thereby supporting a primate colonisation of Madagascar from
Africa [8], but proposed mechanisms for this transoceanic colonisation have been highly
controversial. Here I cite evidence from several recent studies that suggest a likely
mechanism for a successful colonisation across the formidable water barrier of the
Mozambique Channel.
Three hypotheses have been proposed to explain the presence of primates and ter-
restrial mammals on Madagascar long after its separation from Africa: (1) island-hop-
ping across the Mozambique Channel after a temporary reduction in sea levels [9],
(2) invasion during the presence of a temporary land bridge [10] and (3) rafting on
drifting vegetation [11, 12]. The geological evidence concerning the presence of a chain
of islands or even a continuous land bridge during these periods is still incomplete and
controversial [7, 10]. Moreover, the first two hypotheses fail to provide a satisfactory
explanation for the small number of terrestrial mammalian taxa that successfully colon-
ised Madagascar. The rafting hypothesis has been dismissed on the grounds that lemurs
and other small mammals were not physiologically suited for a successful crossing of the
Lemur Origins
Folia Primatol 2000;71:422–425
423
more than 400 km wide channel [3, 10, 13], but successful over-water dispersal is highly
probable over geological times [14] and has been confirmed for other vertebrates [15,
16].
The Extended Rafting Hypothesis
Several independent studies recently provided pieces of evidence relevant for the
reconstruction of the primate colonisation of Madagascar and suggest a plausible mech-
anism for successful rafting. First, phylogenetic analyses of mitochondrial DNA
sequences and an extensive morphological data set demonstrated a single origin for
Malagasy primates [8], followed by rapid cladogenesis, which makes a single successful
colonisation event sufficient to explain the present distribution and diversity of lemurs.
Second, a composite estimate of primate phylogeny suggested that the mouse and dwarf
lemurs (Cheirogaleidae) are the most ancestral group among the living lemurs [17].
Third, mouse (Microcebus spp.) and dwarf (Cheirogaleus spp.) lemurs have long
been known to enter daily torpor or month-long hibernation during the cool austral
summer [18–20, see also 21, 22]. Recent physiological studies in the field demon-
strated that these lemurs actually reduce their metabolic rates by up to 90% and lower
their body temperatures close to ambient temperatures, thereby saving around 40% of
their average daily energy expenditure [23]. Finally, field studies of individually
marked cheirogaleids revealed that mouse and dwarf lemurs typically spend daily and
seasonal periods of inactivity in aggregations of up to 15 individuals in single tree holes
[24, 25, see also 26, 27], thereby further enhancing their energy savings [28]. Because of
the phylogenetic position of these taxa, it is most parsimonious to assume that this
combination of behavioural and physiological traits was also shared by the ancestral
lemurs [12].
Together, the results of these studies provide indirect evidence for the rafting
hypothesis for the primate colonisation of Madagascar by suggesting a plausible mecha-
nism for a successful migration. Accordingly, it is less likely that ‘a pop-eyed ancestral
lemur clung with all its hands onto the wave-washed twigs of a raft of floating tree trunks
or tangled branches’ [11, see also 13], but rather that entire groups of animals survived
the weeks [16] or even months of such a journey without food and water sleeping in a
hollow tree while rafting across the sea. Moreover, according to this scenario the initial
demographic and genetic bottleneck would have been much wider because of the arrival
of several individuals at the same place and time, making a successful colonisation
much more likely.
Successful rafting of more or less inactive individuals could also explain the pres-
ence of other major mammalian groups on Madagascar. The insectivores of the family
Tenrecidae have low metabolic rates and several of them hibernate for months [29].
Similarly, some Herpestidae and Viverridae are among the most hypometabolic carni-
vores [30]. The physiological traits exhibited by these unrelated taxa may have been
advantageous during extended voyages across open seas, thereby explaining a large pro-
portion of the composition of today’s mammalian community on Madagascar. In addi-
tion, the Asian lorises, which must have also originated in Africa [31, 32], have some of
the lowest metabolic rates among primates [33], suggesting the possibility that their
ancestors may have reached Asia also by rafting. A recent phylogenetic analysis, how-
ever, suggested an Asian origin for Madagascar’s endemic rodents, followed by a subse-
424
Folia Primatol 2000;71:422–425
Kappeler
quent secondary invasion of Africa [34], indicating that the Eocene exchange of mam-
mals among Africa, Asia and Madagascar was not limited to one particular direction
[35].
Acknowledgments
I thank Nick Davies, Steve Goodman, Carola Borries, Eckhard Heymann and Caroline Harcourt
for stimulating discussions, helpful suggestions and for their comments on an earlier version of the
manuscript.
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... Given the disjunction between the reconstructed divergence dates of living mammal clades and the continental drift histories of Africa and Madagascar, biogeographers have had little choice but to revert to the old "fixed-continent" models of inter-continental dispersal (Darlington, 1957;Simpson, 1940). Transoceanic journeys on rafts of vegetation have become, once again, the only imaginable means of Madagascar's colonization by Cenozoic clades of terrestrial animals (Ali & Huber, 2010;Ali & Vences, 2019;Kappeler, 2000;Krause, 2010;Krause et al., 2020;Mahé, 1972;Martin, 1972;Nagy et al., 2003;Quammen, 1996;Samonds et al., 2012Samonds et al., , 2013Stuenes, 1989;Vences et al., 2004;Yoder, 1996;Yoder et al., 2003;Yoder & Nowak, 2006). ...
... Mammal waifs are, hence, proposed to have survived in floating hollow trees or on mats of vegetation in a state of hibernation (Martin, 1972;Yoder, 1996). Some animals hibernate in family groups (McNab, 2002), which would facilitate the establishment of viable populations after making landfall (Kappeler, 2000). Seasonal hibernation (May-September) has been observed in lemurs (Blanco et al., 2018;Dausmann et al., 2004; and tenrecs (Lovegrove & Génin, 2008;Treat et al., 2018), and is known to occur in rodents and carnivores in other parts of the world (McNab, 2002). ...
... Thus, the use of torpor is invoked as having increased the probability of surviving a transoceanic crossing for four of the orders of terrestrial mammals that arrived on Madagascar during the Cenozoic (Ali & Vences, 2019;Kappeler, 2000;Martin, 1972;Yoder, 1996;Yoder et al., 2003), but not for hippopotamuses. ...
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... Given the disjunction between the reconstructed divergence dates of living mammal clades and the continental drift histories of Africa and Madagascar, biogeographers have had little choice but to revert to the old "fixed-continent" models of inter-continental dispersal (Darlington, 1957;Simpson, 1940). Transoceanic journeys on rafts of vegetation have become, once again, the only imaginable means of Madagascar's colonization by Cenozoic clades of terrestrial animals (Ali & Huber, 2010;Ali & Vences, 2019;Kappeler, 2000;Krause, 2010; 5. In the case of mammals, with high metabolic demands, the waifs coped with thirst and starvation by entering a state of hibernation during the voyage. ...
... Mammal waifs are, hence, proposed to have survived in floating hollow trees or on mats of vegetation in a state of hibernation (Martin, 1972;Yoder, 1996). Some animals hibernate in family groups (McNab, 2002), which would facilitate the establishment of viable populations after making landfall (Kappeler, 2000). Seasonal hibernation (May-September) has been observed in lemurs (Blanco et al., 2018;Dausmann et al., 2004; and tenrecs (Lovegrove & Génin, 2008;Treat et al., 2018), and is known to occur in rodents and carnivores in other parts of the world (McNab, 2002). ...
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... Simpson, 1980;O'Dea et al., 2016). Notably , 1860 1870 1880 1890 1900 1910 1920 1930 1940 1950 1960 1970 1980 1990 2000 2010 2020 Sclater Wallace Jacobi Fooden Gaffney & Forster Vidal 1910192019301940195019601970198019902000 PublicaƟon date et al. et al. et al. et al. et al. et al. et al. et al. et al. et al. Fig. 2. Chronological summary of the key literature explaining the arrival of the bulk of Madagascar's land-bound vertebrate clades. ...
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Thesis
Protected areas (PAs) are a key aspect of biological conservation. In the past, PAs tended to be selected opportunistically, which sometimes led to inefficient reserve systems. Systematic conservation planning (SCP) scientifically assigns areas for reserves to meet specified conservation targets. The effectiveness of the PA network in Madagascar for lemur conservation was evaluated using Marxan (SCP software). Species ranges were predicted using Maxent (species distribution modeling software). Range maps were compiled to produce diversity estimates and used to inform species target settings for Marxan. An optimal reserve solution was generated and compared with the existing network. There was an overlap of only 50% indicating that the existing network is inefficient. An alternative solution based on expanding the current PA network was also generated. Only 29% of lemurs are adequately represented by the existing network. Expansion of the PA network by 142% is necessary to meet all conservation targets.
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Schon die ersten Naturforscher, die Madagaskar besuchten, erkannten die Besonderheit dieser „Schatzinsel der Natur“. Auf Schritt und Tritt begegneten sie unbekannten Tieren, die so exotisch waren, dass sie sie mit Worten aus ihrer Welt nicht zu benennen wussten. Die Madagassen hatten sie wohl aus demselben Grund oft einfach nach den Lauten benannt, die sie von sich gaben: Sifaka, Fossa, Tenrek, Aye-Aye oder Vanga. Der französische Botaniker und Mediziner Philibert Commerson wähnte sich sogar im „Gelobten Land für Naturforscher“. Bis heute hat sich am Staunen der Biologen nichts geändert, denn die Tier- und Pflanzenwelt Madagaskars ist nur mit Superlativen zu beschreiben. Der einsame Vorposten vor der Ostküste Afrikas ist die viertgrößte Insel der Welt und umfasst mit 587.000 Quadratkilometern etwa die Fläche Frankreichs. Dieses relativ kleine Areal ist allerdings bewohnt von fünf Prozent aller beschriebenen Tier- und Pflanzenarten der Erde. Bemerkenswert ist zudem, dass die Mehrzahl dieser Arten endemisch ist, also einzig und allein auf Madagaskar vorkommt. Alle Amphibien und Säugetiere (bis auf wenige vom Menschen eingeführte Arten), 92 Prozent aller Reptilien, 44 Prozent aller Vögel, 74 Prozent aller Schmetterlinge und mehr als 90 Prozent aller Pflanzenarten sind nirgendwo sonst auf der Welt zu finden (Goodman und Benstead 2005). Diese Vielfalt und Einzigartigkeit von Flora und Fauna zeichnen Madagaskar als „Megadiversitätsland“ aus, ein Status, den weltweit nur zwölf Länder erreichen, die mehr als zwei Drittel der auf der Erde lebenden Arten beherbergen (Myers et al. 2000).
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Until now, the field of primate genomics has focused on two major themes: understanding human evolution and advancing biomedical research. We propose that it is now time for a third theme to receive attention: conservation genomics. As a result of anthropogenic effects, the majority of primate species have become threatened with extinction. A more robust primate conservation genomics will allow for genetically informed population management. Thanks to a steady decline in the cost of sequencing, it has now become feasible to sequence whole primate genomes at the population level. Furthermore, technological advances in noninvasive genomic methods have made it possible to acquire genome-scale data from noninvasive biomaterials. Here, we review recent advances in the analysis of primate diversity, with a focus on genomic data sets across the radiation. Expected final online publication date for the Annual Review of Animal Biosciences, Volume 9 is February 16, 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
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Organisms expend energy for a variety of tasks, including body maintenance, movement, resource acquisition, courtship, reproduction, and growth. Energy expenditure is greatest in species that have high costs of maintenance (e.g., endotherms), high activity levels (due either to extended periods of activity or to the use of expensive forms of locomotion, such as flight and elaborate courtship rituals), expensive means or extended periods of resource acquisition, high rates of reproduction, high postnatal growth rates, and extended periods of parental care.
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Energetic benefits provided by sharing a nest were investigated by measuring resting metabolic rate in the lesser mouse lemur (Microcebus murinus), a nocturnal solitary primate that usually groups in a nest during its diurnal rest. Resting metabolic rate was measured on 32 individuals maintained either alone or grouped with one, two, or three conspecifics originating from the same social group. In this seasonal breeder, individual resting metabolic rate varied significantly from 1.08 +/- 0.03 to 1.47 +/- 0.05 (SE) ml O-2 h(-1) g(-1) for nonbreeding and breeding seasons, respectively. During the breeding season, both sexes reduced their energetic expenditure by 20% when grouped in pairs, and maximal energetic benefit (40%) was achieved when three animals nested together. During the nonbreeding season, maximal energetic gain was observed when as few as two animals nested together because resting metabolic rate was already decreased. Finally, when three or four animals shared the same nest, resting metabolic rate was minimal, independent of sex and season, at 0.88 mi O-2 h(-1) g(-1), suggesting that nest-sharing in this solitary primate is an important strategy to minimize energetic costs to cope with seasonal shortage of food.
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Resting metabolic rate (RMR) and body temperature ( TbT_{b} ) were measured in the shrew-tenrecs Microgale dobsoni and Microgale talazaci during reproduction. Limited data are also presented for Microgale cowani and Microgale melanorrhachis. Resting metabolic rate and TbT_{b} fluctuated with ambient temperature ( TaT_{a} ) so that metabolic rate in nonbreeding animals could not be termed "basal." Resting metabolic rate in nonreproducing adults of all four species at 30°C was higher than levels previously recorded in the Tenrecidae. The smaller species had RMR higher than predicted by the Kleiber curve. During pregnancy and lactation, elevated levels of RMR were attained in M. dobsoni, M. talazaci, and M. cowani, but there was no evidence that the level of RMR attained was influenced by litter size. All three species demonstrated improved thermoregulation during pregnancy. It is concluded that a high level of RMR is advantageous, and possibly essential, for reproduction in the Tenrecidae. Elevated RMR may be associated with an improvement in homeothermy.
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Phylogeny is the study of the real genealogical relationship of taxa. It is not fully knowable. Phylogenetic trees combine information from fossil forms, from living species, from dating, from anatomy, and from chemistry, but none of these fields can stand alone in reconstructing phylogeny. Neither dendrograms grouping extrapolated dates of dichotomies with present-day species nor phylogenetic trees including only fossil forms placed on noncommittal side branches are adequate. Molecular biology can be seen as one field contributing to the understanding of phylogeny, but in no sense should it be viewed as overthrowing or supplanting the evidence from other disciplines. Dendrograms with branch-point dates extrapolated from presently living species can contribute to understanding phylogeny in some cases, but such charts are devoid of historical content, that is, the names, the nature, and the way of life of the fossil forms themselves. In addition, many splitting-time dendrograms, for primates at least, bear little relation to the record left by extinct members of this order. A definite problem exists in resolving these two major sorts of approaches.
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Although Darwin’s ideas concerning the factors and forces responsible for the generation of diversity varied somewhat from one edition of The Origin of Species to the next, by the time he came to write the sixth edition his thoughts had crystallized (Darwin, 1872, p. 129): “Although isolation is of great importance in the production of new species, on the whole I am inclined to believe that largeness of area is still more important, especially for the production of species which shall prove capable of enduring for a long period, and of spreading widely. Throughout a great and open area, not only will there be a better chance of favourable variations, from the large number of individuals of the same species there supported, but the conditions of life are much more complex from the large number of already existing species; and if some of these many species become modified and improved, others will have to be improved in a corresponding degree, or they will be exterminated. Each new form, also, as soon as it has been much improved, will be able to spread over the open and continuous area, and will thus come into competition with many other forms.” (our emphasis)