Basic Research
My research interests fall into two major areas: understanding evolution and relationships of major invertebrate groups at deeper levels and understanding processes producing patterns of biogeography in marine and estuarine invertebrates. Marine invertebrates are unique in that their evolution and biogeographic range are are causally intertwined with their developmental process. The broad array of adult invertebrate morphologies are a direct result of the developmental pathways expressed in larval and postlarval development, and the timing and mode of this development (e.g., planktotrophy or lecithotrophy) indirectly influences dispersal in the environment and ultimately can affect a species' biogeographic range.
In recent years, my work and that of my students has focussed on molecular meiofanual genetics. Most recently, we have begun to assess the toxicity of fipronil. For the past 20 years, one of the most lethal and commonly used insecticides in coastal agriculture, golf course developments and tract housing termite control has been the organophosphate chlorpyrifos (trade name Dursban). Unfortunately, undesirable childrens´ health effects from chlorpyrifos have emerged in the past five years that have lead to its ban for homeowner use and to regulatory disfavor by the USEPA and applicators in general. As a replacement, the USEPA has licensed and recommended widespread use of the "modern" organochlorine: fipronil. Fipronil is one of the most persistent, lipophilic and toxic insecticides licensed for use since dieldrin, lindane and DDT. Surprisingly, fipronil was licensed with a very limited dataset of non-target toxicological effects on estuarine and marine fauna (US EPA Office of Pesticides, pers. comm.). Yet, fipronil is a strong neurotoxin that acts at the broad, phylogenetically conserved level of the GABA receptor. Environmentally, fipronil has a high affinity for sediment carbon and organismal lipid and a half-life of > 5 years (Hainzl and Casida 1996). These features place sediment-dependent meiobenthos and macrobenthos at especially high risk for negative population impacts from this fipronil exposure.
Fipronil is being used increasingly on golf courses of the south Atlantic bight as an EPA-mandated replacement for control of organophosphate-resistant (Diazinon and Dursban) mole crickets. The persistence of this compound provides satisfactory control of mole crickets with three or fewer applications per year (e.g., spring and summer). Human health concerns linked to chlorpyrifos exposure in the home have also led to increasing fipronil application as a replacement for soil-amended control of domestic termites, cockroaches, and carpenter ants (e.g., sold over the internet at http://www.doyourownpestcontrol.com/fipronil.htm or over the counter in products such as Maxforce FCTM). In South Carolina, the Charleston County municipal golf course uses fipronil for turf grass management, as do several golf courses on Hilton Head Island (National Ocean Service, unpubl.).
In the lab of David K. Jacobs, we investigated the expression of homeobox genes (such as engrailed) to assess fine-scaled cell differentiation in the larvae of marine worms and molluscs using in situ hybridization. The Jacobs' lab uses RT-PCR to generate cDNA sequences for these genes not only for their subsequent use in in situ hybridization, but also for exploring phylogenetic relationships among spiralian taxa. Information gleaned from their later use to derive developmental expression of these body patterning genes provides new insight to homology of classical developmental characteristics, which have been used historically to construct the evolutionary patterns within invertebrates.
Using degenerate primers, I amplified, cloned and sequenced a 232 bp fragment of engrailed (inclusive of the homeobox region) for the following taxa: Apionsoma misakianum, Sipunculus nudus and Themiste lageniformis, sipunculan worms (1 clone each); Urechis caupo, an echiuran worm (1 clone); Emerita talpoideum and Callichirus major, crustaceans (1 clone each); and Bipalium kewense, a free-living flatworm (3 clones). Preliminary results of in situ hybridization experiments on Haliotis suggested that engrailed activity was localized in the region forming the shell gland (24-h postfertilization trochophores), which has been suggested previously for the larvae of the mud snail Illynassa and similarly occurs at the posterior margins of the shell plate origins of Lepidochiton (Jacobs et al. 2000). Expression patterns in the 14-d trochophore larvae of the echiuran Urechis caupo are localized in paired ventral ganglia, suggestive of patterns previously reported in leeches.
Unfortunately, almost nothing is known of fipronil´s effects on invertebrate non-target species in estuarine receiving waters. Our present Sea Grant funded research assesses the emerging fipronil hazard to these systems. The high toxicity, persistence and bio-accumulation potential of fipronil place it at the forefront of significant emerging threats to the SE coastal zone.
Figure 1: Fipronil degrades photochemically (hn) under environmental conditions to the desulfinyl derivative as the major photoproduct and the detrifluoromethylsulfinyl, sulfone, and sulfide compunds as minor products (from Hainzl and Casida 1996).
Past Sea Grant funded research has focussed on the development of an estuarine nematode model of toxicity. This research will utilize new information from the Caenorhabditis genome project, which nears completion, to develop genetic markers that respond directly to pollutants. Although the seemingly most distant from my research emphasis to date, the effects of coastal urbanization has and will continue to impact and alter species' genetic composition and biogeography. Understanding these xenobiotic stressors and their role in microevolutionary processes is not only important from a toxicological and management standpoint but will define new understanding of the selective regimes imposed upon estuarine invertebrates. (Photo courtesy of AWI-Bremerhaven)
I collaborated with Damhnait McHugh and Edward B. Cutler on a revision of the phylum Echiura, worldwide at Harvard University in Cambridge, MA. By combining a morphologic reassessment of the taxonomic groups and creating a morphological phylogenetic hypothesis, the groundwork is laid for beginning and molecular systematic treatment of the echiuran worms possibly using the small subunit ribosomal (18S) sequence and exploring collaborative work on elongation factor alpha.
During a NSF post-doctoral fellowship in the laboratory of Wesley M. Brown, I worked on techniques to isolate mitochondrial DNA and collected small subunit (18S) ribosomal & cytochrome c oxidase 1 sequences to help resolve relationship within and among the Sipuncula, a phylum of marine, non-segmented worms. Sipunculans have been hypothesized to have closest common ancestry with two different protostome phyla, the Annelida and Mollusca. Analyses of classical larval morphology have produced ambiguous results (Cutler, 1994- Fig 1). I initially turned toward comparative molecular studies for this group, since there are so few morphologic characters which may be used to form a phylogenetic hypothesis of ancestry at the phylum level for these groups.
At the species level, physical characteristics of the environment and aspects of larval ecology and adult physiology interact to produce patterns of biogeographic distribution in benthic, marine invertebrates. Major ocean currents transport the mobile larvae of essentially sessile adults differing distances dependent upon length of development during their pelagic existence. If the larvae can survive transport, find suitable habitat to settle, and reproduce, the genetic continuity can be maintained between sites. The greater the larval development time, the greater the distance over which this can be accomplished, and the larger the potential range of a marine invertebrate. However, changing local conditions, geographic barriers (physical or physiologic), or competition can potentially limit the full realization of adult range for a larva with potentially long-distant dispersal (i.e., long development time).
The analysis of genetic variation within and among populations of animals provides insight into levels of gene flow among populations and elucidates the success or failure of dispersal and recruitment among the different regions within a species' biogeographic range. I studied these patterns in detail as part of my dissertation research on crustacean phylogeography in the Caribbean, Gulf of Mexico and Southern Atlantic Bight. Fuller understanding of the nature of genetic variation within species provides insight into evolutionary patterns among species, aspects of conservation biology, and the estimation of biodiversity, itself.
In my work on Apionsoma, a widespread sipunculan taxon with teleplanic (far-wandering) larvae, it was possible to note that larval dispersal in and of itself does not explain modern genetic patterns for the species. Larval dispersal does not enhance gene flow because cryptic genetic groups occur that do not appear to interbreed-- even though larvae of one group are able to disperse into the habitat of the other.
Updated 9 December 2002