Unusual Phenotype Suggests Role for Homeotic Genes in Arachnid Development

3 Pages·1999·2.6 MB·English

by  Jessica E Garb

1999. The Journal of Arachnology 27:539-541
RESEARCH NOTE
UNUSUAL PHENOTYPE SUGGESTS ROLE FOR HOMEOTIC
GENES IN ARACHNID DEVELOPMENT
Studies of segmental mutations in Dro- sults in two rear-thoraxes instead of one front
sophila melanogaster have led to the discov- and one rear thorax, causing flies to have two
ery ofseveral classes ofregulatory genes im- pairs of wings instead of one pair of wings
portant in determining body pattern (Carroll and one pair of halteres. In organisms other
1995). These regulatory genes are also than Drosophila, genetic mechanisms under-
known as transcriptional factors because their lying body plan development are less well un-
proteins bind to another gene’s control re- derstood and have only recently been inves-
gions, or promoters, allowing for controlled tigated in arachnids (Damen et al. 1998;
expression or repression. For example, at- Telford & Thomas 1998).
tachment of maternal effect gene transcripts Recently, I collected an immature Misu~
to specific areas of an ovum in Drosophila, menops sp. (Thomisidae) on the Hawaiian Is-
initiates the anterior-posterior (AP) body axis land of Maui which showed a dramatic seg-
(Melton 1991). Diffusion of maternal effect mental mutation. It was collected from wet
proteins from opposing ovum poles creates a forest in the Nature Conservancy’s Waikamoi
dual concentration gradient that differentially preserve on east Maui. This individual closely
activates or represses additional classes of resembled Misumenops anguliventris Simon
transcriptional factors. This cascade of reg- 1900, one of 17 described species of Misu-
ulatory gene expression determines position- menops endemic to the Hawaiian Islands.
al information, indicating body polarity and Thomisids are one of the few spider families
regional specificity. containing genera that are known to be excep-
Regional specificity within body plans is tionally diverse in the Hawaiian archipelago
largely determined by a class oftranscription- (Gillespie 1994).
al factors known as homeotic genes. Specific After closer examination of this individual
concentrations ofmaternal effect proteins turn under a light microscope, I noticed a second
on different homeotic genes controlling the set of eight eyes on its abdomen. These “ab-
identity of segments along the AP axis of an dominal eyes” displayed the exact pattern of
arthropod’s body. Remarkably, homeotic the eight “normal” eyes on the cephalothorax.
genes are arranged on chromosomes in linear In addition, the dorsal aspect of the abdomen
clusters corresponding to their exact sequence displayed the same type and pattern of setae
of expression. Those located toward the left also found on the carapace of the cephalotho-
end ofthe complex are expressed in posterior rax. Despite these dramatic morphological ab-
parts of the body, while those to the right are errations, the posterior aspect of the abdomen
expressed toward the anterior parts (Kenyon resembled a “normal” abdomen. At the time
1994). of collection, the spider was a third or fourth
Bithorax (BX-C) andAntenapedia(ANT-C) instar juvenile. It lived for two months and
are the two known complexes of homeotic appeared typical in behavior. After death, the
genes. ANT-C in Drosophila controls the spider was preserved in 70% alcohol and was
identity of appendages (Carroll 1995). A mu- then prepared and examined using a Hitachi
tant ANT-C gene causes flies to grow a leg in S-800 scanning electron microscope (see Figs.
their antennae socket. BX-C in Drosophila 1,2). The specimen has been deposited in the
controls the morphology of the posterior tho- Bishop Museum entomological collections.
rax and abdomen. A mutant BX-C gene re- Kaston (1982) summarized accounts of oc-
539
540 THE JOURNAL OF ARACHNOLOGY
—
Figure 2. Illustration of anomolous Misumen-
ops sp. thomisid. PME = posteriormedianeyes,CP
= cephalothorax, AD = abdomen.
—
Figure 1. Scanning electron micrograph of
anomalous Misumenops sp. thomisid, dorso-lateral turn on an entire group of regionally inappro-
view. priate homeotic genes. Alternatively, dupli-
cation ofanterior structures might arise ifma-
ternal nurse cells placed transcripts activating
ular anomalies in spiders. Of the nine cases anterior development at the anteriorend ofthe
he described, only two involved spiders gain- ovum as well as the where the abdomen
ing eyes. These specimens, having 14 and 16 would normally arise. The mutant phenotype
eyes, were explained as a result ofembryonic could also be created through a chromosomal
duplication of a head region. It is premature aberration produced during gametogenesis. If
to suggest that these phenotypes were a result the linear cluster of homeotic genes is dupli-
of a mutation in a major regulatory gene be- cated at the region corresponding to the ceph-
cause there are no accompanying figures alothorax, this mightresultin the development
showing where these eyes were located. Ifad- of two cephalothoraxes.
ditional eyes were located on a segment other Evolution of homeotic genes may explain
than the cephalic, this confusion in segment the immense diversity of body forms seen
identity would strongly suggest abnormal ho- among arthropods (Kenyon 1994; Carroll
meotic gene expression. 1995). Small mutations in these highly con-
The “abdominal” eyes and duplicated se- served genes result in macro-mutations, pro-
tation pattern shown in the spider I collected viding an evolutionary mechanism for gener-
may be explained by several different hypoth- ating novel phenotypes. Homeotic genes have
eses. First, a mutation in a homeotic gene of also been identified in cnidarians, nematodes
the bithorax complex may account for the ab- and annelids. Most recently, homeotic genes
normal phenotype. However, homeotic muta- have been identified in a spider (Damen et al.
tions are expressed in individual segments and 1998) and mite (Telford & Thomas 1998).
because spider abdomens are composed of Comparative investigation of homeotic gene
several segments, generation of this pheno- expression will undoubtedly play an important
type would require independent mutations in role in understanding the evolution of arach-
all segments. It is more likely that this mutant nid morphology.
was produced because the wrong set of ho- I thank Tina Carvalho, Marilyn Dunlap,
meotic genes was turned on, while the correct Steve Robinow, Randy Haley, Rosemary Gil-
set was not. This could be brought about by lespie and Cherry Ann Rivera for assistance
several mechanisms. A mutation in a regula- in preparing this note and the Nature Conser-
tory gene determining body polarity might vancy for access to the collecting site.
garb—UNUSUAL ARACHNID PHENOTYPE 541
LITERATURE CITED Lewis, E.B. 1978. Agenecomplexcontrollingseg-
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479-485. mal formation. Science, 252:234-241.
Damen, W.G.M., M. Hausdorf, E.A. Seyfarth & D. Telford, M.J. & R.H. Thomas. 1998. Expressionof
Tautz. 1998. A conserved mode of head seg- homeobox genes shows chelicerate arthropods
mentation in arthropods revealed by the expres- retain their deutocerbral segment, Proc. Natl.
sion pattern ofHox genes in a spider. Proc. Natl. Acad. Sci., 95:10671-10675.
Acad. Sci., 95:10665-10670.
Gillespie, R.G. 1994. Hawaiian spiders of the ge- Jessica E. Garb: Department of Zoology
nus Tetragnatha. III. Tetragnatha acuta clade. J. and Center for Conservation Research and
ArachnoL, 22:161-168.
Training, University ofHawaii, Edmundson
Kaston, B.J. 1982. Additional ocular anomalies in Hall, Honolulu, Hawaii 96822 USA
spiders. J. Arachnol., 10:279-281.
Kenyon, C. 1994. If birds can fly, why can’t we?
Homeotic genes and evolution. Cell, 78:175- Manuscript received 30 May 1997, revised 9 No-
180. vember 1998
.