Access Type

Open Access Dissertation

Date of Award

1-1-2010

Degree Type

Dissertation

Degree Name

Ph.D.

Department

Biological Sciences

First Advisor

Aleksandar Popadic

Abstract

ABSTRACT

UNRAVELING THE MOLECULAR MECHANISMS OF INSECT DIVERSITY

by

STEVEN MICHAEL HRYCAJ

April 2010

Advisor: Dr. Aleksandar Popadic´

Major: Biological Sciences

Degree: Doctor of Philosophy

While it has long been recognized that the arthropods represent the most diverse animal phylum, the molecular bases defining these large-scale differences in body plans and appendages are only now becoming clear. Specifically, the recent merger between the fields of evolutionary and developmental biology ("evo-devo") have provided several examples illustrating that this extraordinary diversification may be due to evolved variation(s) in the developmental networks that control the formation of these structures. In addition, the delineation of such developmental processes can provide a fresh, unbiased perspective on the robustness of the more traditional relationships within the arthropods that are based on the presence or absence of key group-defining features. For example, evo-devo type studies have determined that all arthropod mandibles are gnathobasic (composed of coxapodite only) and therefore, this feature can no longer be used to more closely group the insects and myriapods to the exclusion of the crustaceans. This result illustrates how evo-devo analyses can effectively establish true homologies of complex morphological traits.

All insects possess a tri-partite body plan that consists of a head, thorax and limbless abdomen. Therefore, it would seem likely that the developmental networks controlling the establishment of these three regions would also be conserved. However, we have found lineage-specific variation in the genetic mechanisms that act to maintain one of these key insect features. Specifically, our analyses show that the POU homeodomain gene nubbin (nub) plays a critical role in the establishment of the limbless abdomen via the up-regulation of the hox gene abdominal-A (abd-A) in the milkweed bug (Oncopeltus fasciatus) that is not present in Drosophila. Hence, these data indicate that there are at least two independent mechanisms that act to maintain the establishment of the limbless abdomen in insects. In a similar fashion, we also show that the formation of the dorsal ridge, a highly conserved structure that separates the head and thorax in all insects, may also be maintained by at least two independent molecular mechanisms. In the cockroach Periplaneta americana, the embryonic abolishment of the hox gene Sex combs reduced (Scr) disrupts this ancient boundary, and results in the formation of an ectopic, supernumerary segment between the head and thorax. Interestingly, while Scr mutants Tribiolium yield an identical phenotype, no such ectopic segment develops when Scr is abolished in either Oncopeltus or Drosophila. Hence these data collectively indicate that a fair amount of plasticity may exist in the developmental networks controlling the establishment of class-defining insect features.

Previous studies have indicated that the hox genes are required for conveying segmental identity along the antero-posterior axis in insects. However, while the post-embryonic functions of these genes have been well characterized in holometabolous lineages such as Drosophila, virtually no data exist about their roles during post-embryogenesis in more ancestral, hemimetabolous species. Briefly, the hemimetabolous mode development differs from the holometabolous mode in that the first nymph that hatches from the egg at the end of embryogenesis phenotypically resembles the eventual adult. Therefore, the question remains that if the majority of adult phenotypes are already established during embryogenesis, what are the functions of the hox genes during post-embryogenesis in hemimetabolous lineages? Our analyses of Scr in two hemimetabolous lineages (Oncopeltus and Periplaneta) identified novel temporal and spatial differences of function during embryonic and post-embryonic development. Specifically, in both instances the embryonic role of Scr is mainly restricted to the head with no role in the prothoracic (T1) segment. Conversely, during post-embryogenesis, Scr solely functions to provide identity to the T1 segment and has no major role in the head region in either species. In addition, the post-embryonic abolition of Scr in both Oncopeltus and Periplaneta results in the growth and formation of ectopic wings that originate from the paranotal tissue of the dorsal pronotum. This result suggests that the role of Scr in suppressing the normally active wing program on T1 appears to be conserved in both holo- and hemimetabolous insects. Overall, these findings provide important new insights into the current debate on the morphological origin of insect wings.

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