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The origin of the T. cruzi clade

Two main hypotheses have been proposed for the origin of the T. cruzi clade and T. cruzi cruzi itself.82962 The first proposal based on phylogenetic evidence placed the origin of the T. cruzi clade in the southern supercontinent of Gondwana, comprising present day Antarctica, Australia, and South America, when marsupials were the dominant mammalian fauna, more than 45 million years ago.8 This hypothesis was supported by the existence of two species that are restricted to terrestrial mammals in South and Central America, T. cruzi and T. rangeli, and the placement of a trypanosome from an Australian kangaroo within, but on the periphery of the clade8; Stevens et al.8 termed this group the “T. cruzi clade.” As both T. cruzi and T. rangeli are genetically diverse, they are likely to have had a long history within the New World. Additionally, other Schizotrypanum trypanosomes had been described from other South American terrestrial vertebrates1 suggesting a diversity of related species existed in the continent. According to this hypothesis, the ability of bats to disperse by flying is responsible for spreading bat-trypanosome lineages within the clade to the Old World.8,70

Barnabe et al.130 proposed an alternative, in which T. cruzi evolved from a trypanosome of bats and adaptation of T. cruzi to other mammalian hosts is a derived character that was acquired from a bat-restricted ancestor. This scenario was inferred from evidence of a close relationship between T. cruzi and a range of bat trypanosomes in an analysis of isoenzymes, random amplified polymorphic DNA, and cytochrome b nucleotide sequences. Later this hypothesis gained further support through surveys of bat trypanosomes and phylogenetic studies based on 18S rDNA and gGAPDH sequences. These increased the known diversity of bat trypanosomes within the T. cruzi clade and resolved relationships in the group. Indeed, the closest living relative of T. c. cruzi is T. c. marinkellei (from South American bats), followed by T. erneyi, from bats in Mozambique, Africa,67 and T. dionisii, from both Old and New World bats.8134766131 Explaining the distribution of bat trypanosomes in the clade at the time using the southern supercontinent hypothesis would have required at least seven independent host switches from terrestrial mammals into bats.124 The existence of several terrestrial lineages interspersed with bat trypanosomes in different branches of the T. cruzi clade led to the “bat seeding hypothesis”.124 In this scenario bats were the original hosts of the T. cruzi clade. These trypanosomes then diversified and dispersed in bats, achieving a transcontinental distribution. Several jumps into terrestrial mammals occurred, including one that led to T. cruzi in South American terrestrial mammals. Other jumps into terrestrial mammals led to T. rangeli in South America, the Australian mammal group, the African monkey and civet trypanosomes 62 and the recently described Madagascar lemur group.63

Recent studies have added further support to a probable bat origin of the group. In particular, a number of surveys of trypanosomes of bats in Africa and South America has considerably increased the known genetic diversity of bat trypanosomes within the T. cruzi clade.64,123,129 Notably, T. livingstonei, a trypanosome described in African bats, falls basal to the Australian kangaroo group within the T. cruzi clade.123 Likewise, T. wauawu, and T. spp. Neobats, recently described from South American bats, formed a sister group to the Australian marsupial group.64 A comparison of the nucleotide diversity of cytochrome b (cytb) in T. cruzi marinkellei, the subspecies restricted to bats, revealed higher diversity within this subspecies than any other T. cruzi subgroup, suggesting it to be the oldest T. cruzi subgroup.132

These findings raise the question of whether further host switches of bat trypanosomes in the T. cruzi clade into terrestrial mammals have occurred. Interestingly, a trypanosome morphologically resembling T. cruzi has been described in the slow loris (a primate) in Malaysia133; to date, all trypanosomes morphologically similar (typical Schizotrypanum morphology) to T. cruzi have demonstrated a close relationship with T. cruzi. Unfortunately, however, the molecular data required to test this are not currently available.

It is also notable that, despite an increasing number of studies that have characterized trypanosomes from a wide range of South American terrestrial mammals using molecular techniques, no further bona fide species within the T. cruzi clade have been discovered in terrestrial mammals from this continent. This apparent low level of diversity does not accord with what might be expected if T. cruzi-group trypanosomes had been present in the continent for at least 40 million years, a key aspect of the southern supercontinent hypothesis. For example, some parasite cultures identified as Trypanosoma leeuwenhoeki (from a sloth, Choloepus hoffmanni) and Trypanosoma minasense (from a neotropical primate, the squirrel monkey, Saimiri boliviensis) on the basis of morphology turned out to be Trypanosoma ran- geli when classified in 18S rDNA genes trees.66 Other recently described parasites from the region have also fallen outside the T. cruzi clade including the “real” T. minasense from primates,90 T. caninum from dogs,134 T. terrestris from a lowland tapir,61 and T. lewisi-like trypanosomes from captive south American primates.135

Several attempts have been made to date the origin of T. cruzi using gene sequence data. Most have relied on the calibration points provided by the southern supercontinent hypothesis. For instance, the separation of Africa and South America, which occurred approximately 100 million years ago, has been used to date the split between the T. brucei and T. cruzi clades.8,29 Similarly, the separation of Australia from Antarctica/South America, which occurred approximately 80—45 million years ago, has been used to date the spilt between the kangaroo trypanosome from the rest in the T. cruzi clade. 28 Under the alternative bat seeding hypothesis,124 the bat origin of T. cruzi clade trypanosomes necessitates that the parasites evolved after the diversification of bats. The fossil record for bats is poor, but molecular dating places the first major split approximately 55 million years ago, and not more than 70 million years ago.136 However, there is no guarantee that parasite evolution and diversification of the T. cruzi clade trypanosomes proceeded at the same rate as the diversification of their bat hosts, and we might expect that the radiation/evolution of the trypanosomes lagged behind that of their hosts. The timing of host—parasite coevolutionary relationships has been the focus of much research, , but bona fide examples from nature that are uncomplicated by host switching, lineage extinction events, etc. are surprisingly hard to find.139 Nonetheless, we might still anticipate that some species within the T. cruzi clade are “younger” than their bat hosts.

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