Monophyly v paraphyly

When Li et al reconstructed the ancestral FoxP2 amino acid sequences for representative lineages of yinpterochiropterans and yangochiropterans it proved to be identical to the archetypal sequence found in most mammals - after excluding fruit bats.

Supporters of bat monophyly seem to have been deceived by one of nature's most spectacular examples of convergent evolution.

In FOXP2, molecular geneticists have finally acquired a scalpel to dissect out the deepest evolutionary relationships within the microchiropterans, and to test whether the supposed relationship between rhinolophoid microbats and fruit bats is real, or, as Pettigrew argues, an artefact of a mutational bias common to all species that fly, including insects, birds and mammals.

The former conclusion makes little sense: if the major lineages of microbats share a common ancestor, how can fruit bats be related to just one lineage - rhinolophoids - but not the others?

Pettigrew posted a commentary on the PLoSOne website, titled, FOXP2 Destroys the Microbat Paraphyly Hypothesis: a New Tool for Bat Phylogeny.

He said that the new study was weakened by its assumption that bats are a paraphyletic group - that is, a group in which all species descend from a common ancestor (monophyly), but one clade is separated from the core group.

Reptiles (snakes, lizards, turtles, dinosaurs) are a paraphyletic group, if birds - the descendants of theropod dinosaurs - are placed in Class Aves, but reptiles are a monophyletic group when birds are included.

Pettigrew again argues that microbat paraphyly is an artefact of a mutational bias that arises from the extreme energy demands of flight. The bias loads the genomes of flying creatures - whether mammal, bird or insect - with a surfeit of A-T base pairs.

In DNA hybridization studies, these A-T regions undergo complementary base-pairing purely by chance, and the extra "stickiness" makes fruit bats appear more closely related to microbats than they really are.

Fruit bats appear closely related to Rhinolophoid microbats, which includes the families Hipposideridae (Old World leaf-nosed bats), Rhinolophidae (horseshoe bats) and Megadermatidae (false vampire bats).

Pettigrew believes this apparently close relationship is due to the fact that Rhinilophoid bats, which include most of the larger microbat species in the world, have the highest A-T bias of any microbat group at - rivalling that of fruit bats, which have the highest A-T bias of any mammal (75 per cent).

Remove fruit bats from the Rhinolophoid clade, and take account of the fact that all microbat DNA is also A-T rich, and the major lineages of microbats will also appear to have diverged relatively recently.

If FOXP2 is one of the most highly conserved genes in mammals, Pettigrew says the extreme variation found in the gene in microbats is more likely to reflect an ancient radiation that gave rise to the major lineages of microbats.

Pettigrew notes that while megabats do vary from the standard mammalian FOXP2 "recipe", not one megabat amino-acid substitution is shared with any microbat - not even with their supposed cousins, rhinolophoids.

The microbat variation in FOXP2 is concentrated in two exons of the gene: 7 and 17. Li et al do not provide details of any differences in exon 7, but found that exon 17 is identical to the mammalian consensus sequence.

Unless mutation has run backwards and repaired the mutations, this means megabats cannot be descended from, or related to, rhinolophoid microbats, their supposed sister group within the Yinpterochiroptera. And it is even less likely that they are related in any way to the Yangochipteran microbats.

Pettigrew says the "impressive" divergence of the highly conservative FOXP2 gene in microbats is most likely explain by an ancient origin of microbats - much earlier than 50-million year old Icaronycteris, which had wings and cochlears like modern echolocating microbats.

He cites immunological studies of proteins that place the divergence of microbats around 100 million years ago, a figure that accords with the variation found in FOXP2.

And there is also the circumstantial evidence of a 75-million year old noctuid moth fossil that had already evolved a thoracic "ear" to detect ultrasonic bat sonar - mantises, which evolved in the early Cretaceous (~120mya) also have a thoracic ear to detect bat signals.

Pettigrew has his own comparative DNA study of microbats, fruit bats, colugos and primates in press. Until now, nobody had thought to test relationships between these groups, because bat monophyly rules, and Pettigrew's "flying primate" hypothesis was considered heretical.

When last year's comparative DNA study finally linked colugos to primates, the world in which bats evolved just once, wobbled perceptibly on its North American axis. Pettigrew's forthcoming study could overturn it.