Phylogenies inferred from mitochondrial gene orders-a cautionary tale from the parasitic flatworms.

Abstract

[Extract] Mitochondrial genomes have been used in numerous studies to investigate phylogenetic relationships among eukaryotes at many levels (e.g., Smith et al. 1993; Boore et al. 1995; Boore, Lavrov, and Brown 1998). In recent years, the arrangement of genes in the mitochondrial genome has been regarded as a powerful record of historical relationships (Boore 1999). Changes in mitochondrial gene order are infrequent, even over considerable spans of time (Boore 1999), and are unlikely to exhibit homoplasy. Our research has focused on the relationships between two groups of human blood flukes within the genus Schistosoma. Our investigations on the mitochondrial genomes of these worms revealed striking divergences in mitochondrial gene order within the genus. The schistosomes are among the most significant parasites of humans in the developing world. The disease they cause, schistosomiasis, is second only to malaria in public health importance, affecting some 200 million people in 75 countries and giving rise to severe morbidity or mortality in tens of millions. Recent molecular studies (Barker and Blair 1996) have demonstrated that the deepest split in the genus is between East the Asian species utilizing prosobranch snail hosts and the African species utilizing pulmonate snails. The depth of this split has led some authors to propose an early Tertiary divergence (Despres et al. 1992). Species closely allied with the African group also occur in the Middle East, India, and parts of Southern Asia. One African species, Schistosoma mansoni, was probably introduced into the Americas by the slave trade during the 18th and 19th centuries (Despres, Imbert-Establet, and Monnerot 1993). The Asian group contains fewer recognized species, and these are found primarily in East Asia (the Philippines, China, Malaysia, Indonesia, Cambodia, and Laos). There is a growing realization that African and East Asian schistosomes differ in many biological attributes, including morphological characters, infectivity to snails, range of definitive hosts, growth rates, egg production, prepatency periods, pathogenicity, and immunogenicity (McManus and Hope 1993). We expected our investigations of mitochondrial genomes in these two groups of species to provide more evidence of their phylogenetic distance. However, we were startled by the remarkable differences in mitochondrial gene order which came to light between the two groups and which we report here.