Molecular phylogeny and divergence times of Malagasy tenrecs: Influence of data partitioning and taxon sampling on dating analyses
© Poux et al; licensee BioMed Central Ltd. 2008
Received: 01 August 2007
Accepted: 31 March 2008
Published: 31 March 2008
Malagasy tenrecs belong to the Afrotherian clade of placental mammals and comprise three subfamilies divided in eight genera (Tenrecinae: Tenrec, Echinops, Setifer and Hemicentetes; Oryzorictinae: Oryzorictes, Limnogale and Microgale; Geogalinae:Geogale). The diversity of their morphology and incomplete taxon sampling made it difficult until now to resolve phylogenies based on either morphology or molecular data for this group. Therefore, in order to delineate the evolutionary history of this family, phylogenetic and dating analyses were performed on a four nuclear genes dataset (ADRA2B, AR, GHR and vWF) including all Malagasy tenrec genera. Moreover, the influence of both taxon sampling and data partitioning on the accuracy of the estimated ages were assessed.
Within Afrotheria the vast majority of the nodes received a high support, including the grouping of hyrax with sea cow and the monophyly of both Afroinsectivora (Macroscelidea + Afrosoricida) and Afroinsectiphillia (Tubulidentata + Afroinsectivora). Strongly supported relationships were also recovered among all tenrec genera, allowing us to firmly establish the grouping of Geogale with Oryzorictinae, and to confirm the previously hypothesized nesting of Limnogale within the genus Microgale. The timeline of Malagasy tenrec diversification does not reflect a fast adaptive radiation after the arrival on Madagascar, indicating that morphological specializations have appeared over the whole evolutionary history of the family, and not just in a short period after colonization. In our analysis, age estimates at the root of a clade became older with increased taxon sampling of that clade. Moreover an augmentation of data partitions resulted in older age estimates as well, whereas standard deviations increased when more extreme partition schemes were used.
Our results provide as yet the best resolved gene tree comprising all Malagasy tenrec genera, and may lead to a revision of tenrec taxonomy. A timeframe of tenrec evolution built on the basis of this solid phylogenetic framework showed that morphological specializations of the tenrecs may have been affected by environmental changes caused by climatic and/or subsequent colonization events. Analyses including various taxon sampling and data partitions allow us to point out some possible pitfalls that may lead to biased results in molecular dating; however, further analyses are needed to corroborate these observations.
The Malagasy tenrecs belong to the Afrotheria, one of the four basal clades of placental mammals which have recently been recognized . This ancient group of African origin is divided into two clades: the strongly supported Paenungulata, composed of the orders Sirenia (sea cows), Proboscidea (elephants) and Hyracoidea (hyraxes), and the Afroinsectiphillia , comprising the orders Afrosoricida (golden moles and tenrecs), Macroscelidea (elephant shrews) and Tubulidentata (aardvark) [3, 4]. The tenrec family (Tenrecidae) comprises four subfamilies, the Potamogalinae from continental Africa, and the Tenrecinae, Geogalinae and Oryzorictinae from Madagascar. The Malagasy tenrecs are divided into eight genera and 30 species [5–8]. Based on morphology, tenrecs were previously grouped in the insectivorous order Lipotyphla, which has turned out to be biphyletic and now is split into the orders Eulipotyphla (hedgehogs, moles, shrews, solenodons) and Afrosoricida .
The Malagasy tenrecs have diversified into a spectacular radiation in terms of morphology, behavior, physiology and ecology. They show a high degree of adaptation to their niches (terrestrial, semi-arboreal, fossorial and semi-aquatic) and considerable convergence with other insectivores, notably shrews and hedgehogs. This made it difficult to understand the origin and phylogenetic relationships of this group on a morphological basis. The Tenrecinae (spiny tenrecs) include four genera (Hemicentetes, Tenrec, Setifer, Echinops), characterized by a spiny pelage and a large body size compared to the other tenrecs. Their monophyly is well established, even at the morphological level . The branching of the four remaining genera (Geogale, Oryzorictes, Limnogale and Microgale), which share a shrew-like appearance and a small size, remains more open. Most earlier, molecular studies did not include more than five tenrec species [11–15], while Poux et al.  missed the large-eared tenrec (Geogale). Therefore, not all relations between and within the three subfamilies of Malagasy tenrecs have yet been firmly established. Only two recent studies, by Olson and Goodman  and Asher and Hofreiter , included all tenrec genera, but were unable to confidently resolve the position of Geogale, which suggests the necessity to expand the number of species and sequences for this family.
The island of Madagascar is a well-known biodiversity hotspot, displaying diverse and highly endemic amphibian, reptilian and mammalian faunas. The level of endemism reaches 95% for the non-flying vertebrates, and this level is mainly due to a few speciose endemic radiations [19–21]. Four clades of terrestrial endemic mammals are present, the lemuriform primates, the euplerine carnivores, the nesomyine rodents and the Malagasy tenrecs. Each of these clades represents one unique event of colonization from continental Africa, followed by several diversification events that gave rise to the actual Malagasy diversity [16, 22]. The colonization of a new environment can be followed by an adaptive radiation, defined as a rapid succession of speciation events leading to a high ecological and phenotypic diversity within a lineage . The study of adaptive radiations on islands or in lakes is essential for understanding processes of speciation and diversification [24–26]. Therefore, knowing the patterns and timing of the successive diversification events within endemic island clades, which, like tenrecs, display a broad ecological and morphological diversity, might help to better understand this phenomenon.
Apart from Echinops telfairi, for which the genome sequencing is in progress, there are only a limited number of sequences available in public databases to reconstruct a solid molecular phylogeny of the Malagasy tenrecs. In the present study we therefore selected exons from four independent nuclear genes that are widely used in mammalian phylogeny (ADRA2B, AR, GHR and vWF) in order to resolve tenrec phylogeny. This study is especially focused on understanding the phylogenetic position of the large-eared and the web-footed tenrecs, Geogale and Limnogale, respectively. In addition, we used a relaxed molecular clock timeframe to compare tenrec evolutionary patterns with defined adaptive radiation characteristics. Moreover, the influence of both taxon sampling and data partitioning on the accuracy of the estimated ages were assessed.
Results and Discussion
Within the paenungulate clade the Tethytheria (elephants + sea cows) are strongly supported by morphological and complete mitochondrial genome data [33, 34]. Nuclear genes are ambiguous about this relationship and left the phylogenetic affinities between the three paenungulate orders essentially unresolved [1, 14, 35, 36]. Our concatenated tree shows for the first time, based on nuclear genes, strong support for one of the three possible hypotheses: the grouping of Hyracoidea with Sirenia (PP = 0.99 and BP = 89). Bootstrap trees supporting alternative hypotheses exclusively group elephant with hyrax (BP = 11); Tethytheria is never recovered. All four genes independently support this result; the high support for the sea cow + hyrax grouping is therefore expectedly due to the synergy of these non-conflicting informations. To test whether our extensive taxon sampling within Tenrecidae may have improved the phylogenetic accuracy [37, 38], all tenrecs but one (Tenrec ecaudatus) were removed from a new analysis. The results did not differ much; support for the Sirenia/Hyracoidea clade dropped negligibly in the concatenated analyses (PP = 0.98 and BP = 86). Interestingly, in a retroposon insertion analysis, Nishihara et al.  found one insertion supporting exclusively the grouping of hyrax with dugong. These authors dismissed the apparent synapomorphous hyrax-sea cow insertion as homoplastic, in favor of the morphological evidence for Tethytheria.
Similarly, the relations between the afroinsectiphillian orders have not yet been clarified, and conclusions vary in different studies. Mitochondrial data give highly inconsistent results [34, 39], while mixed data tend to group golden moles and tenrecs with elephant shrews, together being the sister group of aardvark, with rather strong support [1, 35, 40]. Our data also support these results, as the Afrosoricida/Macroscelidea clade (= Afroinsectivora) is displayed with high confidence (PP = 1.00 and BP = 93), and Tubulidentata is found to be the sister group of this clade (PP = 1.00 and BP = 95). With a smaller dataset (only one tenrec) the support for the Afrosoricida/Macroscelidea clade slightly increased (PP = 1.00 and BP = 96). Hence, enlarged taxon sampling cannot explain our strong phylogenetic results within the afrotherian clade. All four genes separately displayed Afroinsectiphillia either as paraphyletic or weakly supported therefore the present results are not due to gene sampling biases. The retroposon analyses of Nishihara et al.  proposed the grouping of golden moles, tenrecs and aardvark, to the exclusion of elephant shrews, on the basis of two shared retrotransposons.
Phylogenetic position of Geogale aurita
The large-eared tenrec (G. aurita) has been included until now in only two molecular studies, by Olson and Goodman  and by Asher and Hofreiter . These two studies found two different results concerning its phylogenetic position. The first study, comprising three mitochondrial genes (ND2, 12s rRNA and tRNAvaline) and one nuclear marker (vWF exon 28), displayed, in a parsimony framework, the large-eared tenrec as the most basal of all Malagasy tenrecs. This result was not influenced by the inclusion of morphological characters in the analyses. Asher and Hofreiter , using exon 10 of the GHR gene and morphological data, found Geogale nested within the Oryzorictinae, as sister group of the Microgale/Limnogale clade.
Results of the Shimodaira-Hasegawa test.
Geogale sister group of Oryzorictinae
Asher and Hofreiter (2006)
Geogale nested within the Oryzorictinae
P = 0.287
Olson and Goodman (2003)
Geogale sister group of all other Malagasy tenrecs
P < 0.001
Ks and Ka calculated for each pair of Malagasy tenrec GHR sequences.
M. cf. parvula
Further phylogenetic analyses of the GHR dataset, including both Geogale sequences or removing all segregating sites between the two sequences, led to the same result as obtained by Asher and Hofreiter , i.e. Geogale nested within the Oryzorictinae. The phylogenetic position of Geogale as sister group of Oryzorictinae was only obtained when our sequence alone was used. However, both Geogale sequences always grouped together, confirming the identity of our sequence. These results, in combination with the fact that the Oryzorictinae/Geogalinae clade radiated very fast, might make it difficult to reach a final consensus on the evolution of Geogale.
From a morphological point of view the phylogenetic relation between Geogale and the Oryzorictinae has never been clear. Although most studies gave unresolved results [, Olson  in [17, 18]], two were concordant with ours [42, 43], while none has ever argued that Geogale was either the sister group of all Malagasy tenrecs or the sister group of the Limnogale/Microgale clade. Salton and Szalay  reached the conclusion that the tarsal morphology of Geogale warrants its status as a separate subfamily, and suggested its closer affiliation with Oryzorictinae than with Tenrecinae.
Three genera of fossil tenrecids – Erythrozootes, Protenrec and Parageogale – from the Kenyan and Namibian Miocene (16–24 Mya; Million years ago) have been discovered until now [44–46]. As Parageogale is thought to be the sister group of the extant Geogale aurita , these data would suggest a more complex dispersal history than the "one time dispersal event" deduced from the monophyly of Malagasy tenrecs. Asher and Hofreiter  were the first to include these three fossil tenrecids in a phylogenetic framework. Their result confirmed the position of the Kenyan fossils as Geogale's closest relatives. However, alternative hypothesis (e.g., monophyly of the Malagasy tenrecs) could not be ruled out indicating the uncertainty of the Parageogale/Geogale affinity. Recent studies have argued that the sweepstakes dispersal model (dispersal with small and random probability of success) from Africa to Madagascar suffers from many inconveniences, among which the fact that prevailing winds and currents between Africa and Madagascar would be much more likely to favor transports from the island to the African continent, rather than the reverse route [47, 48]. Therefore, if a second dispersal event ever occurred it was most probably from Madagascar to Africa. Olson and Goodman  suggested a basal position of Geogale among Malagasy tenrecs and argued that, if true, this would only imply a minimum of two dispersal events, whereas any other scenario would require at least three. However, a back dispersal of Parageogale from Madagascar to Africa would only assume a second dispersal event, independent of the phylogenetic position of Geogale.
Phylogenetic position of Limnogale mergulus
Due to its semi-aquatic life style, shared with the African Potamogalinae, the determination of the phylogenetic relationship of Limnogale, the web-footed tenrec, has led to controversies. Its specialized morphological features brought some authors to the conclusion that Limnogale was either sister group of the Potamogalinae  or sister group of all other Malagasy tenrecs , the semi-aquatic behavior then being seen as an ancestral state and a key element to facilitate over-water dispersal. In contrast, other morphological studies challenged this view by affirming that Limnogale had closer relationships to the shrew tenrecs (Microgale), and that the semi-aquatic behavior was an example of convergence acquired twice during tenrec evolution [Guth et al. in , Olson  in ]. This strong affinity between Limnogale and Microgale has recently also been supported by a study of hind limb muscles . These authors argue that Limnogale may have been derived from a Microgale-like terrestrial ancestor. Molecular studies have now confirmed this last hypothesis [16–18]. Supporting the hypothesis of Olson and Goodman , our study shows that the semi-aquatic Limnogale is actually nested within the shrew tenrec genus and not a sister clade of it (Figure 1), now with more elaborate analyses and strong support from four nuclear genes.
The phylogenetic supports displayed in the present study are quite low, even with the concatenated dataset (PP = 0.67 and BP = 59), probably due to the fact that the Microgale/Limnogale clade may have radiated very fast (Figure 1). Only one gene, GHR, presents a high PP of 0.99 for the cluster of Microgale cf. parvula/Limnogale mergulus (Figure 2). The sequencing of more shrew tenrec species (a total of 21 species has been recorded [5–8]) might help to resolve this issue, and subsequently to understand the morphological evolution of the aquatic specialization of the web-footed tenrec.
Tenrec diversification timing
Comparison of estimated Malagasy tenrec divergence times (in Mya).
Clade and node number
This study 9 partitions
This study without GHR
Age ± SD
Age ± SD
Age ± SD
Age ± SD
63 ± 5
67 ± 5
69 ± 4
71 ± 4
Malagasy tenrecs/Potamogalinae, 2
43 ± 5
42 ± 4
47 ± 4
45 ± 4
Malagasy tenrec radiation, 3
25 ± 3
29 ± 3
30 ± 3
Tenrecinae radiation, 4
16 ± 3
18 ± 2
20 ± 2
21 ± 3
Tenrec/Hemicentetes split, 5
13 ± 2
16 ± 2
15 ± 2
Setifer/Echinops split, 6
6 ± 1
7 ± 1
8 ± 2
Geogalinae/Oryzorictinae split, 7
24 ± 3
24 ± 3
Oryzorictinae radiation, 8
19 ± 3
22 ± 3
22 ± 3
Microgale radiation, 9
11 ± 2
11 ± 2
Microgale/Limnogale split, 10
9 ± 1
9 ± 2
Posterior estimates of divergence times (Mya ± standard deviation) inferred from the concatenated datasets.
Calibration time frame (Mya) a
This study without GHRb
79.1 ± 4.7
73.5 ± 4.8
75.5 ± 4.3
55.6 ± 3.1
54.7 ± 3.0
53.3 ± 2.4
73.7 ± 4.0
77.3 ± 3.9
76.5 ± 3.6
To exclude the possibility that individual calibration constraints may bias our dating analyses, we repeated them after removing each calibration point in turn following . Hereby we could check whether the excluded calibration constraint was accurately estimated by the remaining ones. All datings remained highly congruent when any of the six calibration points was removed. The average percentage difference between the main analysis and the ones with only 5 constrained nodes ranges between 0.1 and 0.8 percent. Only the paenungulate calibration seems to have a somewhat larger impact on the dating as its removal from the analysis increases the estimated node age by 4.8 percent. This influence is however too slight to have an impact on our conclusions (Additional files 1 and 2). Moreover, the calibrations were reciprocally compatible: the remaining five calibrations always recovered a posterior estimate (± SD) for the excluded node within the time window independently obtained from the corresponding fossil evidence (Additional files 1 and 2).
Since Geogale has been hypothesized by Olson and Goodman  to be the first Malagasy tenrec genus to have diverged, its absence from Poux et al.  was a problem for drawing final conclusions about tenrec colonization timing. It now appears that Geogale is nested within the Malagasy tenrec clade, and therefore plays no role when estimating the period of colonization. Consequently, the window of colonization of Madagascar by tenrecs could not be narrowed. As previously concluded in Poux et al. , the tenrec colonization time completely overlaps with the hypothetical time of existence of a land bridge crossing the Mozambican channel (26–45 Mya; ) (Figure 3), which however is highly controversial .
Taxonomic sampling and accession numbers of the four nuclear genes.
Lepus sp. 2
Tupaia sp. 4
Equus sp. 6
Lama sp. 7
Microgale cf. parvula
Macropus sp. 14
Even though the colonization of Madagascar by tenrecs might have taken place during the Eocene, the radiation of the extant species started after Madagascar reached its current geographical subtropical location during the early Oligocene , with warmer climatological conditions probably similar to the actual ones . The colonization of Madagascar by carnivores and rodents took place at the end or just after the Oligocene, around 20–23.5 Mya for rodents, and 19–26 Mya for carnivores (data taken from  in order to compare results inferred from similar datasets and methods). These dates are quite close to the periods of appearance of extant tenrec genera: the radiation of Tenrecinae and the split between Tenrec and Hemicentetes occurred 20 ± 2 Mya and 16 ± 2 Mya, respectively; Geogale split from the Oryzorictinae 24 ± 3 Mya; and Oryzorictes separated from Microgale 22 ± 3 Mya. So five out of the seven tenrec genera (Limnogale is taken here as a Microgale) diverged soon after the colonization of Madagascar by carnivores and rodents. These new colonizations may have altered the ecological conditions, and thereby induced speciation within tenrecs, either by predation pressure (carnivores) or by interspecific niche competition (rodents).
The complete phylogeny of the Malagasy tenrec genera has now been resolved with strong support. These results should lead to a revision of the taxonomy with regard to the genus Geogale (if it comprises more than one species) and the Limnogale/Microgale clade (if this last genus is truly paraphyletic). This solid phylogenetic and dating framework shows that the major morphological specializations of the tenrecs are not the result of fast adaptive radiations just after colonization, but would as well have been affected by ecological changes caused by climatic and/or subsequent colonization events; however, more work is still needed to understand the role of possible biotic interactions on the speciation processes of Malagasy tenrecs.
Sampling, DNA amplification and sequencing
Fragments of the intronless gene of the alpha 2B adrenergic receptor (ADRA2B), of exon 1 of the androgen receptor (AR) gene, of exon 10 of the growth hormone receptor (GHR) gene, and of exon 28 of the von Willebrand factor (vWF) gene were amplified and sequenced. These genes were selected because (i) they are located in the nuclear genome, as single-copy genes (in at least human and mouse), (ii) a considerable number of sequences are already available for all four genes and have been useful in mammalian phylogeny, and (iii) they are functionally and genetically unrelated. We selected for each of the four genes 38 mammalian species to represent (i) all genera of Malagasy tenrecs, and at least two species of the very diverse genus Microgale, in order to assess the phylogenetic position of Limnogale, (ii) the continental African sister group (Potamogalinae) of the Malagasy tenrecs, (iii) groups needed for multiple calibrations of the molecular clock, (iv) at least one species from each eutherian order (but for Pholidota), and (v) appropriate marsupial outgroups. A total of 19 new sequences were obtained, and complemented with 134 sequences from GenBank (Table 5).
Genomic DNA was isolated from ethanol-preserved tissue, following the protocols of the Wizard® SV Genomic DNA Purification System (Promega). Fragments of the ADRA2B and AR genes were amplified using previously published primers [16, 57]. New primers were designed for vWF and GHR (see Additional file 3). For these last genes PCR reactions were performed on 50–200 ng DNA with Expand DNA polymerase (Expand High Fidelity PCR system, Roche) using the following program: 2 min at 94°C; 30–35 cycles of 15 sec at 94°C, 1 min at 60°C and 1 min 30 sec at 72°C; and a final step of 2–10 min at 72°C. DMSO (1.3 – 2.5%) and/or betaine (1 M) was added for some samples. PCR products were purified from a 1% agarose gel, using GFX™ PCR DNA & Gel Band Purification Kit (GE Healthcare), and reamplified if necessary. Gel-extracted PCR products were sequenced directly on a 3730 96-capillary sequencer (Applied Biosystems). Internal primers were used to get complete sequences of both strands.
Best fitting evolutionary model for each codon position.
Estimated by MODELTEST
Estimated by PAML
TRatio or Rmat
(1.0 2.5 0.7 0.7 2.5)
(1.6 6.1 0.7 2.6 3.6)
(1.2 4.4 2.5 0.4 4.4)
(1.0 4.5 0.5 0.5 3.0)
(1.2 2.9 0.7 1.8 2.9)
(1.0 5.4 0.7 0.7 4.4)
(2.1 3.9 0.9 1.1 2.8)
(1.0 6.0 0.8 0.8 3.8)
(1.7 3.4 1.1 1.3 3.4)
(1.0 5.6 1.0 1.0 4.3)
(2.5 9.9 5.6 0.8 9.9)
To assess the stability of the phylogenetic position of Geogale aurita, our result was compared, according to both Kishino and Hasegawa  and Shimodaira and Hasegawa  (using RELL bootstrap as well as full optimization methods), to the hypotheses of Olson and Goodman  and Asher and Hofreiter . Furthermore, Ka (i.e., number of nonsynonymous substitutions per nonsynonymous site) and Ks (i.e., number of synonymous substitutions per synonymous site) of pairwise tenrec sequences were calculated using the program CODEML from the PAML package  in order to assess the molecular divergence between the two Geogale GHR sequences and compare it with the level of molecular divergence displayed within the Malagasy tenrec clade.
We used the Bayesian approach  as implemented in the MULTIDIVTIME program package , which relaxes the molecular clock by allowing continuous autocorrelation of substitution rates among the branches of the phylogenetic tree. The concatenated sequence dataset was partitioned into the same nine categories as for the Bayesian phylogenetic analyses, and branch lengths were calculated under the F84 + Γ model of sequence evolution, which is the most complex model available in MULTIDIVTIME. Each of the described analyses was run twice in order to assess the consistency of the results. The prior for the root was set at 100 Mya, however, analyses with 65 Mya, 80 Mya and 120 Mya as prior age were also performed in order to estimate the impact of the root prior on our results. For each node, we calculated the variance of the estimated ages over all the runs. A maximal variance of 2*10-4 was found showing that changing the root prior does not influence age estimates. Markov Chain Monte Carlo analyses were run for 1,000,000 generations after a "burn in" of 100,000 generations. The chains were sampled every 100 generations. To assess the influence of a particular partitioning on the dating results, we performed additional analyses using four partitioning schemes: without partitioning, with nine partitions following the results of MODELTEST, with five partitions following the results of ESTBRANCHES using the F84 + Γ model, and with a maximum number of partitions (i.e., twelve). The results of these analyses were close to each other. Notably, all datings for the nodes of interest remained within the 95% credibility intervals of the datings obtained in the analysis using five partitions.
Six well established fossil constraints on divergence times were used: (i) a minimum of 54 and a maximum of 65 Mya for the base of Paenungulata ; (ii) a minimum of 50 and a maximum of 63 Mya for the split between feliform and caniform Carnivora [45, 68]; (iii) a minimum of 54 and a maximum of 58 Mya for the split between hippomorph and ceratomorph Perissodactyla ; (iv) a minimum of 55 and a maximum of 65 Mya for the base of Cetartiodactyla ; (v) a minimum of 37 Mya for the split between ochotonids and leporids ; (vi) a minimum of 60.5 and a maximum of 100.5 Mya for the divergence time between rodents and primates . To assess the reciprocal consistency of all calibration points we used the cross-validation method described in . In this method each calibration point is removed in turn and the remaining calibration points are used to estimate its age. Calibration points, for which the estimated and paleontological dates are not congruent, are considered as inconsistent and are consequently removed from the analyses.
We are grateful to numerous colleagues who provided samples and useful information, in particular to W.R. Branch, S. M. Goodman, R. Nincheri, J. Patton, and D.R. Vieites. Field work was carried out in collaboration with the Département de Biologie Animale of the University of Antananarivo. We would like to thank the Malagasy authorities for permits. C.P., O.M. and M.V. were supported by grants from the Netherlands Organization of Scientific Research (NWO).
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