A photosynthetic ancestry for all eukaryotes?

CORRESPONDENCE flies (Cyrtodiopsis dalmanni) offers a new sort of test. Sensory exploitation is the idea that ‘selection favors male traits that exploit sensory biases in females’4. These sensory biases are ‘built into the sensory modality being used and may have no intrinsic adaptive value’s, Thus, ‘the female’s sensory system defined the possible evolutionary alternatives for more attractive male traits’6. Proponents of sensory exploitation argue that biases in females’ neural machinery are evolutionarily ancient, antedating the appearance of the male traits they promote. Phylogenetic reconstructions have been used to infer the history of such ‘preexisting’ biases in fish (Xiphophorus)7,8 and frogs (Physa/aemus)4,g, but conflicting phylogenies have resulted in tenuous concIusionsl,lo. Wilkinson and Reillo’s experiment2,3 suggests a different, potentially useful approach. They selected male flies for large (L) or small (S) eye span relative to body size, and examined females’ mate choices after 13 generations. Females from L-lines preferred L males (as did unselected controls), but S-line females preferred S males. These results implied ‘a genetic correlation between female preference and a sexually selected male trait’z, an interpretation that has been disputed11 and defendedI*. Biases in females’ neural machinery that are strong enough to steer male phenotypic evolution should be difficult to alter experimentally. Yet preferences of female C. dalmanni were rapidly reversed as a by-product of selecting for S males, implying that considerable genetic variability underlies their current expression. Sensory exploitation posits that fixed female preferences drive sexual selection. Plasticity in female preferences is not consistent with this hypothesis. Comparative studies using Wilkinson and Reillo’s approach (e.g. Ref. 13) will be useful for clarifying in other species whether or not female preferences represent fixed biases imbedded in their neural machinery.

Paul W. Sherman L. LaReesa Wolfenbarger Section of Neurobiology and Behavior, Cornell University, Ithaca, NY 14853, USA References 1 Shaw, K. (1995) 2 3 4 5

6 7 6 9

10

Trends Ecol. Evol. 10, 117-120 Wilkinson, G.S. and Reillo. P.R. (1994) froc. R. Sot. London Ser. B 255, l-6 Pomiankowski. A. and Sheridan, L. (1994) Trends Ecof. Ewof. 9. 242-244 Ryan, M.J. and Keddy-Hector, A. (1992) Am. Nat. 139, s4-s35 Kirkpatrick, M. (1987) in Sexual Selection: Jesting the Alternatives (Bradbury. J. and Andersson, M., eds), pp. 67-82, Wiley Ryan, M.J. and Rand, AS. (1990) Evolution44. 305-314 Basolo, A.L. (1990) Science 250,808-810 Meyer, A.. Morrissey, J.M. and Schartl, M. (1994) Nature 368, 539-542 Ryan, M.J. and Rand, A.S. (1993) Proc. R. Sot. London Ser. B 340,187-195 Pomiankowski, A. (1994) Nature 368, 494-495

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F., Gerhardt,

H.C. and Butlin. R.K. (1994)

Trends Ecol. Evol. 9, 343 12 Pomiankowski, A. and Sheridan, L. (1994) Trends Ecol. ho/. 9, 343 13 Houde, A.E. (1994) Proc. R. Sot. London Ser. B 256,125-130

A photosynthetic ancestry for all eukaryotes? In their recent TREEarticles, M. Schlegell and S. Brul and C.K. Stumm* stressed the importance of molecular, biochemical and morphological information for the analysis of the complex endosymbiotic events that led to evolution of the various eukatyotic phyla3,4. They review the current evidence that argues consistently for an early branching of microsporidia, parabasalia and diplomonads, which all lack mitochondria3. Laterbranching eukaryotes possess mitochondria, and some phyla are believed to have acquired plastids later on1,3,4. However, the primitive, free-living, microaerophilic amoebomastigote Psalteriomonas lanterna possesses photosynthetic organelles (thylakosomes), although it lacks mitochondria, microbodies and a well-developed Golgi apparatuss. With the trichomonads, it shares the presence of hydrogenosomes and the putative import signal for hydrogenosomal proteins6,7. The DNA sequence of a ferredoxin confirms the primitive status of this organism7. Thylakosomes are sensitive to the triazine derivative Toltrazuril (Baycox@), although classical antenna pigments are absent, and only traces of chlorophyll a can be found. Nevertheless, a low activity of photosystems I and II, and the presence of a highly conserved psbA gene5, establishes the existence of functional, plastid-like organelles. Microsporidians, the most primitive eukaryotes, are sensitive to Toltrazuril tooa, and ultrastructural studies reveal the presence of membraneous organelles in many species. They are similar in appearance to the proplastids and chromoplasts of higher plantsg, but also to the thylakosomes of Psalteriomonass and the plastid-like organelles of apicomplexans that have been called ‘doublewalled vesicles’ or ‘Hohlzylinder’lo. While it has been known for some time that parasitic Apicomplexa, such as Plasmodium and Toxoplasma, harbour a plastid-type genomell,l*, the presence of traces of chlorophyll a bound to the photosynthetic reaction centers could be substantiated only very recentlylo. The presence of a highly conserved psbA gene in Sarcocystis murk has been shown, and the conservation of the herbicide-binding region of the psbA-encoded Dl protein provides the rationale for the herbicidesensitivity of many Apicomplexansl0.13. Phylogenetic analysis of the psbA gene of Sarcocystis muris locates it among the chloroplasts of green unicellular algae like Euglena, Chlorella and Cblamydomonas, in the neighbourhood of heterokont chromophyteslO. A comparable phylogenetic position is occupied by the plastid-encoded rpoB gene of Plasmodium falciparumld, thereby reinforcing the monophyly of the plastids. Therefore, it is likely that the membraneous cytoplasmic structures known from many apicomplexans, and also from Psalteriomonas and certain Microspora, represent

highly specialized, non-green, but functional plastid-like organelles. Evolution of eukaryotes might therefore be characterized by the very early acquisition of cyanelle-like, photosynthetic organelles, since similar organelles are also found in quite a number of primitive, microaerophilic, heterotrophic or parasitic mastigotes15. Oxygenreleasing photoautotrophy might have been the first function of such organelles, and the loss of photoautotrophy was probably a secondary adaptation to heterotrophy or parasitism. Photosynthetic organelles like plastids can provide oxygen needed in biosynthetic and catabolic reactions, and the proto-mitochondrion might have entered a photoautotrophic eukaryotic cell, in order to be as close as possible to the source of the scarce oxygen. And since molecular phylogenetic trees consistently argue that symbiotic protoplastids were acquired only once in evolution, one might speculate whether mitochondrion-bearing heterotrophic organisms like fungi, ciliates and metazoans might have evolved after the loss of their plastid-type organelles. Actually, the p0, in their biotopes had to be high enough to support mitochondrial function in the absence of intracellular oxygen sources.

J.H.P. Hackstein Dept of Microbiology & Evolutionary Biology, University of Nijmegen, Toernooiveld, NL 6525 ED Nijmegen, The Netherlands U. Mackenstedt Lehrstuhl fiir Spezielle Zoologie und Parasitologic, Ruhr-Universitit-Bochum, Postfach 10 21 48, D-44780 Bochum, Germany References 1 Schlegel, M.

(1994) Trends Ecol. Evol. 9, 330-335 2 Brbl, S. and Stumm, C.K. (1994) Trends Ecol.

E/o/. 9, 319-324 3 Gray, M.W. (1992) ht. Rev. Cflol. 141, 233-357 4 Cavalier-Smith, T. (1993) Microbial Rev. 57, 953-994 5 Hackstein, J.H.P. et a/. (1994) fndocflobiol. Cell Res. 10,261 6 LBnge. S.. Rozario. C. and Mtiller. M. (1994) Mol. Biochem. Parasitol. 66, 297-308 7 Brul, S. et a/. (1994) Biochim. Biophys. Acta 1183,544-546 6 Schmahl. G. et al. (1990) Parasitol. Res. 76, 700-706 9 Kowalllk. K.V. and Herrmann, R.G. (1972) Protoplasma 74, l-6 10 Hackstein, J.H.P. et al. (1995) farasitol. Res. 81,207-217 11 Williamson, D.H. et al. (1994) Mol. Gen. Genet. 243,249-252 I2 Palmer, J.D. (1992) Curr. BIO/. 2, 318-320 13 Mehlhorn, H. et a/. (1984) Z. Parasite&d. 70, 173-182 14 Gardner, M.J. et a/. (1994) Mol. Biochem. Parasitol. 66, 221-231 15 Anderson, O.R. (1987) Comparative Protozoology, Ecology, Physiology, Life History, Springer-Verlag

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