The origin of bats (morphology vs. molecules part 2)

prEarlier we looked at the origin of bats comparing DNA models to morphological models following the publication of Meredith (2011).

Gunnell and Simmons (2005) reported, “Morphological data have almost universally placed bats in the group Archonta, together with dermopterans, primates, and tree shrews (e.g., Wible and Novacek, 1988; Beard, 1993; Simmons, 1993, 1995; Szalay and Lucas, 1993; Miyamoto, 1996). Several phylogenetic studies have suggested that bats and  dermopterans are sister taxa (together forming a clade called Volitantia), an arrangement that is appealing since dermopterans are gliding mammals and many researchers believe that bats evolved from gliding ancestors (Wible and Novacek, 1988; Simmons, 1993, 1995; Szalay and Lucas, 1993, 1996). However, an archontan relationship for bats has been strongly questioned in recent molecular studies.”

“Despite seemingly strong morphological evidence, bats have not appeared as a member of either Volitantia or Archonta in any of the more than two dozen molecular studies completed since the early 1990s. Regardless of the genes sampled or the phylogenetic methods used, bats never group with primates or dermopterans;multiple analyses of nuclear and mitochondrial gene sequences have resoundingly refuted the hypothesis that bats are archontan mammals. Instead, molecular studies uniformly place bats in a Laurasiatheria clade (e.g., Miyamoto et al. , 2000; Murphy et al. , 2001; Arnason et al. , 2002; Douady et al. , 2002; Van Den Bussche et al. , 2002; Van Den Bussche and Hoofer, 2004). Within this group, bats most commonly appear as either the sister group or basal member of a cetferungulate clade (which includes pholidotans, carnivores, cetaceans, artiodactyls, and perissodactyls) or as the sister group of a eulipotyphlan clade (including shrews, moles, and possibly hedgehogs). Accordingly, no single order of mammals appears to be the sister group of bats. Instead, bats seem to be derived from primitive mammals (i.e., basal or near basal laurasiatheres) that also gave rise to several other orders.”

So, where do we stand?
With the early Paleocene placental explosion (O’Leary et al. 2013) we have no fossils that link bats with pholidotans, carnivores, cetaceans, artiodactyls, and perissodactyls. Or do we?

And for that matter…
Where do dermopterans and primates come from?

The bat tree
The bat tree, based on morphology, nests bats close to both of these large clades, deriving them from ancient carnivores and within that clade, prehistoric vivverids (basal carnivores not far from occasionally arboreal civets). Despite their placement in the order Carnivora, civets are omnivorous, or, in the case of the Palm Civets, almost entirely herbivorous. The carnassial teeth are relatively underdeveloped.

Gunnell and Simmons (2005) report, “The fact that the most primitive known fossil bats from the early Eocene already possessed most of the derived characters of extant chiropterans (including specializations for powered flight) suggests that more primitive proto-bats were present by the late Paleocene, if not earlier.”

As in birds and pterosaurs, two hypotheses on the origin of flight in bats have been proposed: the ground-up hypothesis and the trees-down hypothesis. The ground-up hypothesis (Jepsen 1970 and Pirlot 1977) posits webbed hands for capturing terrestrial insects, followed by leaping to capture flying insects.

Evidence of a gliding ancestry for bats may be found in their resemblances to dermopterans. These groups have a number of morphological features of the hand, elbow and foot that are related to gliding, flight, and under-branch hanging (Simmons, 1995; Szalay and Lucas, 1993, 1996).

Gunnell and Simmons (2005) conclude: “Proto-bats were most likely arboreal, small, insectivorous, and nocturnal. All known Eocene fossil bats are small-bodied and have dentitions indicative of an insectivorous diet, and proto-bats probably shared these characteristics (for a discussion of bat occlusal morphology see Polly et al. , 2005). Simmons and Geisler (1998) suggested that primitive fossil bats such as Icaronycteris  and Archaeonycteris  were perch-hunting insectivores that preyed on insects found on surfaces rather than capturing aerial insects on the wing. Protobats, lacking the ability for sustained flight, would most likely have had a similar diet.”

“Like dermopterans and many megachiropterans, proto-bats were probably under-branch hangers that employed both hands and feet while hanging (Simmons, 1995). This form of suspension would have allowed small proto-bats to exploit terminal branch leaves in search of insects and would have positioned them for gliding forays between tree branches or separate trees. Proto-bats may also have had some hindlimb specializations (such as some form of tendon locking mechanism; see Szalay and Lucas, 1993; Simmons and Quinn, 1994).”

The war between morphology and molecules
Occasionally morphology does not agree with molecules. And that’s a problem. Ultimately phylogeny must rule. No matter what is happening in their DNA, juveniles more or less resemble their parents. Evolution proceeds in small generational steps.

Maybe the DNA distances are not so great as we think. 
If we look at the pertinent section of the mammal family tree we find that bats are maybe not so far from either proto-primates or proto-ungulates.

Figure 1. Mammal family tree with color showing probable origin of bats, between carnivores and port-ungulates and pro to-primates.

Figure 1. Mammal family tree with color showing probable origin of bats, between carnivores and port-ungulates and pro to-primates.

The Early Paleocene
When so many mammals radiate so quickly without a distinct fossil record we are left with a cave that will echo back what we yell into it. Here (Fig. 1) we find carnivores and proto-ungulates not that far from tree shrews and primates (and for that matter dermoptera (unlisted). Here’s where we’ll find the origin of bats.

Getting Down to the Genus Level
We took the origin of bats back to the extant Ptilocercus, which was a basal proprimate.  The earliest known bats, Onychonycteris and Icaronycteris and the earliest known pro carnivores, like Vincelestes, and likely proprimates extend back to the Early Cretaceous.

Bats and their sisters

Figure 3. Bats and their sisters according to the DNA results of Meredith et al. 2011. Note the rapid branching at the base, which also extends to the base of the primates + dermopterans. 

So, what looks like a huge DNA gap, may be a small one.
At the time that proto-primates diverged from proto-bats and other proto-placentals, there was, evidently, little morphological difference between them, having radiated so recently from a common ancestor, something like Ptilocercus. In this regard, perhaps flying lemurs and bats represent some of the most primitive members of this clade, despite their subsequent DNA departures.

Just trying to find common ground
Such a DNA vs. morphology problem rears its ugly head again in the large reptile tree and its nesting of synapsid mammals closer to diapsid crocs and birds, leaving turtles and lizards + snakes on another branch, but DNA does not bear this out. Not sure how that one will ever be resolved.

I trust DNA. I also trust phylogenetic analysis. There is so much common ground in non-problem areas, I hope to find some common ground in problem areas.

As always, I encourage readers to see specimens, make observations and come to your own conclusions. Test. Test. And test again.

Evidence and support in the form of nexus, pdf and jpeg files will be sent to all who request additional data.

References
Arnason U, Adegoke JA, Bodin K, Born EW, Esa YB, Gullberg A, Nilsson, M, Short RV, Xu X, and Janke A 2002. Mammalian mitogenomic relationships and the root of the eutherian tree. Proc. Natl. Acad. Sci. U.S.A 99: 8151.
Beard KC 1993. Origin and evolution of gliding in early Cenozoic Dermoptera (Mammalia, Primatomorpha). In: Primates and Their Relatives in Phylogenetic Perspective, R. D. E. MacPhee, ed., pp. 63–90, Plenum, New York.
Gunnell, GF and Simmons NB 2005.
 Fossil evidence and the origin of bats. Journal of Mammalian Evolution 12: 209-246 (2005).
Jepsen GL1970. Bat origins and evolution. In: Biology of Bats 1, W. A. Wimsatt, ed., pp. 1–64, Plenum, New York.
Meredith RW et al. 2011. Impacts of the Cretaceous Terrestrial Revolution and KPg Extinction on Mammal Diversification. Science 334:521-524.
Miyamoto MM 1996. A congruence study of molecular and morphological data for eutherian mammals. Mol.Phylogenet. Evol. 6: 373.
Miyamoto MM, Porter C and Goodman M 2000. cMyc gene sequences and the phylogeny of bats and other eutherian mammals. Syst. Biol. 49: 501.
Murphy WJ, Eizirik E, Johnson WE, Zhang YP, Ryder OA and O’Brien SJ 2001. Molecular phylogenetics and the origin of placental mammals. Nature 409: 614.
O’Leary, MA et al. 2013. The placental mammal ancestor and the post-K-Pg radiation of  placentals. Science 339:662-667. abstract
Simmons NB 1993. The importance of methods: Archontan phylogeny and cladistic analysis ofmorphological data. In: Primates and Their Relatives in Phylogenetic Perspective, R. D. E. MacPhee, ed., pp. 1–61, Plenum, New York.
Simmons NB 1995. Bat relationships and the origin of flight. In: Ecology, Evolution and Behavior of Bats, PA Racey and SM Swift, eds., Symp. Zool. Soc. Lond. 67: 27.
Szalay FS and Lucas SG 1993. Cranioskeletal morphology of archontans, and diagnoses of Chiroptera, Volitantia, and Archonta. In: Primates and Their Relatives in Phylogenetic Perspective, R. D. E. MacPhee, ed., pp. 187–226, Plenum, New York.
Wible JR and Novacek JM1988. Cranial evidence for the monophyletic origin of bats. Am. Mus. Novit.v2911: 1.
Wible JR, Rougier GW, Novacek MJ, Asher RJ 2007. Cretaceous eutherians and Laurasian origin for placental mammals near the K/T boundary Nature 447: 1003-1006

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