The ‘hedgehog’ tenrecs: they nest with hedgehogs

This is a think piece.
You’re going to be faced with

  1. a geographically inspired return of the cloaca (proposed heresy) or
  2. MASSIVE convergence involving everything but the cloaca (current and traditional paradigm)

Arguments will be presented.
You decide which is more parsimonious. We may need to bring in the DNA guys here, and I would welcome them! I don’t think such a study involving a wide range of purported and actual tenrecs has been proposed or done yet. Let me know as I am unaware of published work on this subject.

The present problem had its genesis in whale phylogenetic studies.
Earlier, from skeletal data, the the large reptile tree (LRT) nested odontocete (toothed) whales with tenrecs and mysticete (baleen) whales with hippos and desmostylians.

However
current DNA studies do not support the tenrec – odontocete relationship — perhaps because workers used the lesser hedgehog tenrec (Echinops telfairi, Martin 1838, Figs. 2, 3) in their DNA studies. Echinops is traditionally considered a tenrec, but it may not be one based on bones (Fig. 3) and massive homology/convergence with the European hedgehog, Erinaceus (Figs. 1, 3).

Figure 4. European hedgehog, a member of Glires.

Figure 1. European hedgehog, Erinaceus, a member of Glires.

It’s the cloaca that seems to matter most
in tenrec studies. Plus the location: Madagascar.

Figur3 5. Madagascar hedgehog, is not a tenrec, but another member of Glires.

Figure 2. Madagascar hedgehog tenrec, Echinops, perhaps not a tenrec, but another member of hedgehog family within Glires.

There are two extant hedgehog tenrecs (HHTs):
the greater HHT (Setifer = Ericulus setosus) and the lesser HHT (Echinops telfari). Their skulls are not that different from each other, except in size. They have similar skeletons and spines coats. So we’ll focus on the lesser HHT as other workers have done before.

The problem is
the large reptile tree (LRT) nests Echinops rather convincingly with hedgehogs, like Erinaceus, within Glires, not with tenrecs like Tenrec (Fig. 1). Shifting Echinops to the tenrecs adds 30 steps to the LRT. Shifting the entire tenrec clade (ncluding the odontocetes) to the hedgehogs adds only 12 steps.

We’ve seen something like this before
when the purported tenrec, Potamogale (Du Chaillu 1860, Nicoll 1985; extant), the giant otter shrew that was supposed to be a tenrec, instead nested rather convincingly with shrews, far from tenrecs. It, too, has a cloaca.

Maybe it’s because they’re all from Madagascar.
Not sure what it is about that island that takes a perfectly good set of genital and anal openings and reverts them back into a single primitive cloaca. But that appears to be happening here among unrelated taxa, by convergence.

Among mammals
monotremes have a cloaca and that is most likely the primitive condition, as a cloaca is found in all other reptiles. Most marsupials separate the anus and genitals, so no cloaca is present — except in the very derived marsupial moles. Marsupials are basal to placentals according to the LRT, so any appearance of a cloaca in placentals is a reversal. Thus the Madagascar hedgehogs, the African golden moles and giant otter shrews (Potamogale) that redevelop a cloaca are examples of phylogenetic reversals.

So you  have a choice in nesting these purported tenrecs:

  1. Do you follow the bones and other soft (and prickly, Fig. 2) tissue with the exception of the cloaca?
  2. Or do you follow the cloaca alone? Current taxonomy and experts for over a century favor this choice.

To my knowledge,
mtDNA studies have not been conducted yet to resolve interrelationships among tenrecs and other mammals. If Echinops is indeed a hedgehog, then tenrecs have not been genetically tested against odontocetes. In fact, tell me if I’m wrong, but this may be the first time such a study has been conducted on morphology alone. Asher and Hofreiter 2006 stated at the time: “Due in part to scarcity of material, no published study has yet cladistically addressed the systematics of living and fossil Tenrecidae (Mammalia, Afrotheria).”

Echinops was employed by Mouchaty et al. 2000. Echinops might have been used by Meredith 2011 and Song 2012 to nest tenrecs with golden moles (Chrysocloris) as Afrotheres, related to elephants (Elephas) and hyraxes (Procavia). I don’t see any other tenrecs being used in molecular studies.

Echinops was recently employed by
Suarez 2009 in a study of the vomernasal system (VNS). The distribution of both vomernasal pathways in Eutheria was found to be present in rodents and Echinops, but not in other tested eutherians, none of which included other tenrecs. Of course, hedgehogs nest with rodents in the LRT.

Figure 1. The skulls of Erinaceus (above), Echinops (middle) and Tenrec (below), compared. Note the large premaxillary teeth common to all members of the Glires to the exclusion of other clades, including Tenrecidae.

Figure 3. The skulls of Erinaceus (above), Echinops (middle) and Tenrec (below), compared. Note the large premaxillary teeth common to all members of the Glires to the exclusion of other clades, including Tenrecidae. The anterior maxillary tooth of Erinaceus might be a canine, but it is not at the anterior rim of the maxilla, where one expects a canine.

Let’s compare
a hedgehog, a tenrec and the lesser hedgehog tenrec and perhaps you’ll see that a mistake was made over 100 years ago that continues to adversely affect phylogenetic analyses today. Perhaps a member of Glires has been long considered a member of Tenrecidae by virtue of its location, Madagascar, and its cloaca.

The European hedgehog
Erinaceus europaeus (Linneaus 1758; 20-30cm; extant) this omnivore can roll itself into a ball, erecting its spines for defence. Unlike most Glires, the hedgehog does not have a diastema. The jugal is very tiny in this clade.

The lesser hedgehog tenrec
Echinops telfairi (Martin 1838; extant, 13-17 cm) the lesser or pygmy hedgehog tenrec is widely considered a tenrec, but here it nests with hedgehogs and other Glires including rodents. This omnivore is restricted to Madagascar, home of severalt tenrecs. Note the large canines, like tenrecs and unlike hedgehogs. Note the large premaxillary teeth, like hedgehogs and unlike tenrecs. Unlike tenrecs, the ears are prominent. Like tenrecs, the jugal is absent.

Given that the Madagascar mammals with a cloaca
all do some burrowing, I wonder if the genitals and anus retreated beneath the cover of a single opening in order to keep dirt out? If that’s not the answer, I wonder what the common thread is that these unrelated taxa have that caused that primitive trait to reappear? And I wonder if there are any analyses based on morphology that include several tenrecs and other eutherians for comparison? So far I have found none, so the LRT is shedding light where it may be needed.

If Echinops is indeed a hedgehog with a cloaca
then we have to go get some mtDNA from Tenrec to see if it is a good match for odontocete mtDNA. At present, Tenrec has not been tested for its mtDNA, that I know of, so the whale connection question remains open.

While we’re at it it
count the stomachs in Tenrec. Even odontocetes have subdivided stomachs. Let’s find out when that trait appeared.

References
Asher RJ 2007. A web-database of mammalian morphology and a reanalysis of placental phylogeny. BMC Evol Biol. 7: 108-10 online
Asher  RJ and Helgen KM 2010. Nomenclature and placental mammal phylogeny. BMC Evolutionary Biology 10:102 online
Du Chaillu P 1860. Descriptions of mammals from equatorial Africa. Proceedings of the Boston Society of Natural History, 7, 358–369.
Eisenberg JF and Gould E 1970. The tenrecs: a study in mammalian behavior and evolution. Smithsonian Institution Press, Washington, DC. 138 pp. PDF online
Linnaeus C 1758. Systema naturæ per regna tria naturæ, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Tomus I. Editio decima, reformata.
Martin WCL 1838. On a new genus of insectivorous mammalia. Proceedings of the Zoological Socieety, London, 6:17.
Mouchaty SK, Gullberg A, Janke A, Arnason U 2000. Phylogenetic position of the Tenrecs (Mammalia: Tenrecidae) of Madagascar based on analysis of the complete mitochondrial genome sequence of Echinops telfairi. Zoologica Scripta. 2000, 29 (4): 307-317. 10.1046/j.1463-6409.2000.00045.x.
Nicoll M 1985. The biology of the giant otter shrew *Potamogale velox*. National Geographic Society Research Reports, 21: 331-337.
O’Leary, MA et al. 2013. The placental mammal ancestor and the post-K-Pg radiation of  placentals. Science 339:662-667. abstract
Suárez R, Villalón A, Künzle H and Mpodozis J 2009. Transposition and Intermingling of Gαi2 and Gαo Afferences into Single Vomeronasal Glomeruli in the Madagascan Lesser Tenrec Echinops telfairi. PLoS ONE 4(11): e8005. doi:10.1371/journal.pone.0008005

2 thoughts on “The ‘hedgehog’ tenrecs: they nest with hedgehogs

  1. And here’s a prime example of science working by finding congruence of independent variables. Molecular analyses have indeed been performed for tenrecs, such as Poux et al. (2008), which found Echinops groups with Tenrec extremely strongly (six combined nodes each supported by >90% maximum liklihood and >99% posterior probability keep it from non-afrotherians). Note an odontocete, Potamogale and a Eulipotyphla that is mostly Erinaceus are included. Then you look at biogeography, which matches Afrotheria and Tenrecidae. And the cloaca also matches, which as you note really doesn’t make sense as a systematic reversal of every Malagasy ‘insectivore’. The burrowing excuse doesn’t work since moles or the tons of burrowing rodents don’t revert to a cloaca AFAIK.

    As for “MASSIVE convergence involving everything but the cloaca” being our alternative, and ” tell me if I’m wrong, but this may be the first time such a study has been conducted on morphology alone”, you do realize that the Asher and Hofreiter (2006) study you quote right afterwards includes a morphology-only analysis of 126 characters (figure 6)? Echinops groups with Tenrec instead of Erinaceus with a 99% posterior probability. I’d be willing to bet that your analysis designed for a basic amniote tree doesn’t include almost any of the characters used in Asher’s matrix that’s designed to recover placental mammal and ‘insectivore’ relationships, and that your morphological interpretations are off. As an independent source, note Halliday et al.’s (2015) morphology-only analysis of 680 characters found Potamogale to be far from Pakicetus and Rodhocetus.

    So really the question is- Are molecules, biostratigraphy and anatomy as coded by experts (using multiple specimens examined by hand- Appendix 1 of Asher and Hofreiter- 22 Echinops, 13 Erinaceus, etc.) in studies designed to answer this question right, OR are your results as a novice to mammalian anatomy (using images found online) coded in your general amniote matrix good enough to counter that?

    References- Asher and Hofreiter, 2006. http://sysbio.oxfordjournals.org/content/55/2/181.full

    Poux et al., 2008. http://bmcevolbiol.biomedcentral.com/articles/10.1186/1471-2148-8-102

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