2014. Proceedings of the Indiana Academy of Science 123(2):204–216

129TH ANNUAL ACADEMY MEETING1 Presidential Address by Dale D. Edwards2 ‘‘LET’S TALK SCIENCE— OF FRESHWATER MOLLUSKS’’

ACADEMY MEETING WELCOME participating in today’s meeting. We are also Welcome to the 129th Annual Academy very happy to have a handful of young high Meeting! school science students with us today. I encour- The Indiana Academy of Science has had the age you to take time to get to know these young privilege of serving Indiana scientists from people as they move about the meeting. industry and academia, Indiana science educa- At our Luncheon today, in addition to hearing tors, and Indiana graduate and undergraduate from our guest speaker Dr. Jim Bing, we will science students, as well as aspiring young introduce our Academy leadership, welcome our future scientists and the Indiana general public new Academy Fellows, and applaud our 2014 since 1885. With the mission of promoting Awardees. Immediately following lunch, our scientific research, diffusing scientific informa- poster presenters will be standing aside their tion, improving education in the sciences, and posters in Grand Ballroom 1-4 to talk with you encouraging communication and cooperation about their research. Though their posters will between Indiana scientists, the Academy hosted be up for you to view all day, we will be its first Annual Academy Meeting in Indiana- dedicating our attention to their presentations polis in 1885, at the Marion County Court- from 2:00 to 3:10 p.m. We are also truly looking house. From this historic, yet humble beginning forward to hearing Johannah Barry’s Plenary a proud academy was built. There are many Address this afternoon, regarding the ongoing leading scientists in our membership, and many conservation efforts in the Galapagos Islands. who have made the difference in science as we Following Ms. Barry’s Plenary, we will hold know it here in Indiana. a brief, but very important Academy Member- We have a wonderful Annual Meeting ship Meeting. At this meeting, we will hear from planned for you today, resulting in large part our Section leadership who will be meeting with from the generosity of Eli Lilly and Company you this morning (check for the room number Foundation, the W.K. Kellogg Foundation, of your section meeting in the program book). Subaru of America, and the White River State We will also take a few minutes to vote on Park. Today, 160 of you, researchers from the recommended adjustments to our Bylaws, and State of Indiana, will be presenting science in welcome in the incoming Academy President, both oral and poster presentations. Nationally and the newly elected officers and committee recognized guest speakers Dr. James Bing, members, who will officially take on their new a Global Trait Introgression Leader at Dow responsibility June 1. Be sure to join us for AgroSciences, and Johannah Barry, President desserts, soft drinks, coffee, tea, wine, and beer of the Galapagos Conservancy, will be adding to wrap up our meeting this year. to our science conversation. Hot topics will be Earlier this year, Delores Brown, Executive delivered by those on the cutting edge of much Director of the Academy, thought it would be of the conversation of those topics. Workshops a good idea to reinstate an old tradition at the will also be offered for your professional annual meeting. One in which the Academy development, and for the first time this year, President opened the meeting by talking about with the approval of the Department of science. In this case, she asked if I would be Education, professional education credits will willing to talk about my research. I thought it be granted for our Indiana science teachers was a great idea and was happy to oblige. So without further ado, let’s talk science!

1 J.W. Marriott, Indianapolis, IN, 15 March 2014. MITES OF FRESHWATER MOLLUSKS 2 University of Evansville, Department of Biology Evansville, IN 47722; 812-488-2645 (phone), de3@ What I want to do this morning is give evansville.edu. you an overview of some research that I have

204 EDWARDS—MITES OF FRESHWATER MOLLUSKS 205 been doing for the past twenty years or so More than half of the described species are involving the ecology and evolution of water symbionts of freshwater mussels and snails. mites of the genus that live in Indeed, the Latin name Unionicola literally symbiotic association with freshwater mussels means ‘living within mussels’—since ‘cola’ or and snails. ‘icola’ mean ‘to live within’ and ‘unio’ is a name The primary objectives of this talk are as for mussels. follows: 1) to put the genus Unionicola into taxonomic perspective; 2) to provide you with UNIONICOLA LIFE CYCLE a general life cycle of these water mites; 3) to The life cycle of water mites is complex characterize the precise nature of the symbiotic and includes the egg, larva, protonymph, association between these mites and their deutonymph, tritonymph, and adult. Larvae, molluscan hosts; 4) to discuss some of my deutonymphs, and adults are motile, whereas behavioral research involving Unionicola mites protonymphs and tritonymphs are quiescent, and how these studies have changed our transformational stages of the life cycle. The perception about what it means to be a species adults and deutonymphs of most water in the context of these mites; 5) to provide you species are free-living predators. However, with a framework regarding the phylogenetic there are species from the Pionidae and Union- systematics and biogeography of Unionicola icolidae that are symbiotic with freshwater mites; and 6) to leave you with insights gastropods, mussels, and sponges (Mitchell regarding future directions of my research 1955). Although some species of Unionicola program involving these mites. are free-living predators as nymphs and adults and depend on hosts only for sites of oviposi- PUTTING UNIONICOLA MITES INTO tion and post-larval resting stages, most species TAXONOMIC PERSPECTIVE are obligate symbionts of their hosts. Among Mites, or taxonomically speaking the , those species living within mollusks, the females represent a diverse and variable group of arth- deposit eggs in specific tissues (gills or mantle ropods. Three major lineages or superorders of or foot) of the hosts, with larvae emerging in mites are currently recognized: Opilioacari- late spring and summer. The larvae of most formes, Parasitiformes, and Acariformes. The water mites parasitize aquatic insects and in so Acariformes (the mite-like mites) contains over doing acquire nutrition for larval development 300 families and over 30,000 described species. and a primary mechanism for dispersal. Larval Two major lineages of Acariformes are recog- mites of the genus Unionicola utilize chirono- nized, the Sarcoptiformes (Oribatida and Astig- mids and generally locate these insect hosts mata) and (). The during the pupal phase of development (Fig. 1), Trombidiformes represents a diverse assem- but the mechanisms of host location are not blage of mites. The largest and most spectacular well understood. The larvae eventually rein- lineage within Trombidiformes is Parasiten- vade a host mussel, embed in host tissue, and gona, with over 7000 described species of enter a transformational stage from which the terrestrial and aquatic mites. Mites belonging sexually immature nymph emerges (Fig. 1). to several unrelated groups are commonly found The nymph subsequently enters a transforma- in freshwater habitats. However, the true water tional stage from which the sexually mature mites (Acariformes: Trombiformes: Parasiten- adult emerges. gona) or Hydrachnida (5 Hydrachnellae, Hy- dracarina, and Hydrachnidia) represent a series NATURE OF THE SYMBIOTIC ASSOCIA- of extensive adaptive radiations occurring most- TION BETWEEN UNIONICOLA MITES ly in freshwater habitats. Well over 5000 species AND MOLLUSKS of water mites are recognized worldwide, Although Unionicola mollusk mites have representing more than 300 genera and sub- been traditionally recognized as parasites, there genera in over 100 families and subfamilies. is little known about the nutritional depen- Water mites of the genus Unionicola (Acari: dence of these mites on their hosts or the Hydrachnida: ) represent a diverse impact that unionicolids may have on the hosts collection of more than 250 species in some 57 with which they are associated. Baker (1976, subgenera (Edwards & Vidrine 2013) distribut- 1977) provided evidence that U. intermedia ed in freshwater habitats around the world. from Anodonta anatina is capable of piercing 206 PROCEEDINGS OF THE INDIANA ACADEMY OF SCIENCE

Figure 1.—Generalized life cycle of Unionicola. the gills of host mussels with their pedipalps, host mucus, gill tissue, or hemolymph for at allowing them to feed on hemolymph and least part of their nutrition, the effects that mucus. Extensive infiltration of hemocytes into these mites have on a host has not yet been the damaged regions of the host’s tissue may examined in any detail. Laboratory experi- provide these mites with an additional nutri- ments by MacArthur (1989) indicated that tional source (Baker 1976). Observations by long-term exposure of P. cataracta to U. LaRochelle & Dimock (1981) of U. foili from formosa did not significantly alter the host’s Utterbackia imbecillis indicated that these mites shell morphology and composition, or soft- would occasionally penetrate the gills of their tissue mass and biochemical composition. In host using their pedipalps. However, histolog- addition, there was no evidence that short-term ical examination of the midgut of these exposure of P. cataracta to these mites signif- could not definitely conclude that they were icantly altered their ability to move water or feeding on host tissues. More recently (Fisher filter particles. et al. 2000) used both histochemical approaches and immunological assays to confirm that THE POPULATION BIOLOGY OF U. formosa, a sibling species of U. foili, does ADULT MITES indeed ingest mucus and hemolymph from its A polygynous mating system.—One of the mussel host, Pyganodon cataracta. main reasons I became interested in studying Although it is becoming increasingly appar- Unionicola mites was because of their peculiar ent that Unionicola mollusk mites are utilizing population structure. While examining the pop- EDWARDS—MITES OF FRESHWATER MOLLUSKS 207 ulation dynamics of U. foili (formerly identified from the mantle cavity of the host. Since the as U. formosa) from the mussel Utterbackia pioneering work of Welsh (1930, 1931), other imbecilis, my PhD advisor, Ron Dimock, dis- studies have found that the response to light by covered that the density (number of mites/ several additional species of unionicolid mites is mussel) of female mites was positively correlated influenced by the chemistry of the water in with host size. Male U. foili were, on the other which they were examined (e.g., mites are hand, under dispersed among their hosts, with positively phototactic when tested in water that most mussels harboring a single male. This is free of any chemical influence from a host, drastic difference in the density of male and but in the presence of extracts from its host, the female mites was reported for every month of the sign of their response reverses to negative; year, with the mean sex ratio during a two-year Roberts et al. 1978). study period being close to 30 females:1 male Host-specific behavior by Unionicola mussel (Dimock 1985). mites is also evident from studies examining the The persistent female-biased sex ratio re- recolonization of mussel hosts. For example, ported by my advisor, fit together with other when either U. formosa (from the mussel work (Dimock 1983, Edwards & Dimock 1991) Pyganodon cataracta) or its sibling species indicating that male mites are territorial and U. foili (from the mussel Utterbackia imbecillis) aggressive to other males. The behavior by are removed from a mussel and presented with males was characterized as being consistent a choice between P. cataracta and U. imbecillis, with those of a female-defense polygynous I found that adult mites would preferentially re- mating system. Although a female-biased sex enter the host species from which they had ratio appears to be typical for many species of initially been collected (Edwards 1988). The Unionicola (Mitchell 1965; Davids 1973; Baker mechanisms by which Unionicola mussel mites 1987), there is little known about the impact of discriminate among host mussels are not this population structure on the reproductive known. The behavioral studies of LaRochelle biology of Unionicola mollusk mites. Because & Dimock (1981) and Werner (1983) emphasize fertilization among these mites most likely the role of contact chemoreceptors in mediating occurs within the confines of a host mussel host recognition. However, the findings of (Hevers 1978), then establishing and maintain- LaRochelle & Dimock (1981) and the fact that ing this territory would dramatically increase the induction of mite negative phototaxis can a male’s reproductive success. Unfortunately, occur in water modified by mussels clearly we know next to nothing regarding the suggest that it can be mediated by distance structure (e.g., can resident males successfully chemoreception as well. inseminate all females residing inside the Although most studies regarding the speci- mantle cavity of a host mussel?) and dynamics ficity of the host recognition behavior of (e.g., how often are males displaced by other Unionicola mussel mites have involved adults, males during the mating season?) of the mating there have been few attempts to characterize system for Unionicola mollusk mites, making the behavioral specificity during other stages further comments about male mating success (nymphal and larval) of the life cycle. Because it speculative at best (Edwards et al. 2004). is the larvae that initiate an association with Behavioral specificity.—Symbiotic relation- a host mussel (Fig. 1), characterizing the ships between Unionicola mites and their behavior of this stage of the life cycle was molluscan hosts are characterized by a diversity critical in documenting the nature of host of host-influenced behaviors by the mites specificity of these mites. When I examined (Dimock 1988). The first experiments to the behavior of larval U. foili from Utterbackia examine and document these behaviors in some imbecillis and U. formosa from Pyganodon detail were performed by Welsh (1930, 1931). cataracta, (what was then thought to be one Welsh’s (1930) paper reported that the mite species of mite from two different species of U. ypsilophora (probably U. formosa) was host mussels), I found that they preferentially positively phototactic in the absence of any responded to chemical signals from their re- chemical influence of its host mussel, Anodonta spective host mussels, but the pattern of their (now Pyganodon) cataracta, but exhibited responses changed during larval ontogeny negative phototaxis when tested in water (Edwards & Dimock 1995). For example, containing extract of host gill tissue or in water larvae emerging from U. imbecillis that had 208 PROCEEDINGS OF THE INDIANA ACADEMY OF SCIENCE completed their parasitic phase with chirono- of host species and others utilizing one or at mids (what I referred to as post-chironomid most a few species of hosts (Edwards & Vidrine larvae) exhibited negative phototaxis only in 2006). An examination of both interspecific and the presence of water that had been modified intraspecific genetic diversity among host-asso- by U. imbecillis. The host-influenced behavior ciated populations of these mites undoubtedly exhibited by these larvae was absent among will play a valuable role in testing hypotheses mite larvae prior to parasitizing chironomids about current species designations and poten- (what I referred to as pre-chironomid larvae). tially uncover sibling species of Unionicola The changes in the behavior of pre-chironomid mussel-mites. Results of some recent molecular and post-chironomid larvae probably reflected genetic work in my laboratory are beginning to major differences in the life history strategies of bear witness to the predication. A comparison these developmental stages. For example, post- of partial COI sequences between host-associ- chironomid larvae represent the invasive stage ated populations of U. hoesei, a mite that is of the mussel-mite symbiosis. A preferential known to occur in association with many response to a host chemical factor would, species of host mussels throughout North therefore, be expected, especially if it increased America, has revealed a high degree of genetic the likelihood of locating a host. differentiation. Moreover, these differences are Cryptic species of molluscan symbionts.—I within range of the genetic differentiation that was intrigued by the specificity of host discrim- has been observed among previously recog- ination behavior by larval mites between the nized sibling species of Unionicola, including host mussels U. imbecillis and P. cataracta, those in which morphological differences because these findings, coupled to the fact that among species are relatively minor (Ernsting fertilization among these mussel-mites occurs et al. 2008) and those that appear to be only within the confines of a host mussel morphologically indistinguishable (Ernsting et (Hevers 1978), suggested that specific behav- al. 2006). The discovery of cryptic species of ioral responses to mussels could maintain Unionicola mites based on molecular sequence reproductive isolation between mites occurring data has obvious implications regarding esti- with different host species. An examination of mates of biodiversity within this taxon. A the genetic structure of populations of mites failure to recognize cryptic species among from U. imbecillis and P. cataracta using unionicolid mites would also have important allozyme electrophoresis (Edwards & Dimock implications for anyone trying to unravel the 1997) revealed a high degree of genetic differ- nature of co-evolutionary relationships among entiation between these host-associated popu- Unionicola mites and their hosts. lations, including mites from the two species of hosts being fixed for different alleles at three A PHYLOGENETIC BLANK SLATE loci. Edwards & Dimock (1997) concluded that Our understanding of the evolutionary mites from these two species of mussels were relationships among Unionicola water mites is reproductively isolated and thus constituted limited and has largely been derived from good biological species. Mites from P. catar- morphology-based classifications among mem- acta were recognized as U. formosa sensu bers that comprise the group. For example, stricto, whereas mites from U. imbecillis were Vidrine (1996) and Wu et al. (2009) suggested identified as a new sibling species, U. foili. Since that sponge-associated mites of the subgenus this work was published, genetic studies in my Hexatax (formerly Unionicola) represent the lab, including allozyme analysis (Edwards et al. least-derived taxon within the genus. Morpho- 1998, Edwards & Labhart 2000) and DNA logically, these mites closely resemble species of sequence comparisons (Ernsting et al. 2006, free-swimming mites from the genus Ernsting et al. 2008), have been helpful in (Unionicolidae: Piontacinae). Vidrine (1996) delineating additional species of Unionicola subsequently identified 20 groupings of Union- that were, on the basis of traditional anatom- icola subgenera based on sets of shared ical criteria, morphologically indistinguishable. morphological and life-history characters. De- Interestingly, North American Unionicola spite these rather broad assessments of union- mussels-mites are known to exhibit highly icolid systematics, the evolutionary history of variable patterns of host specificity, with some the genus has not been adequately tested using species occurring in association with a long list phylogenetic approaches. EDWARDS—MITES OF FRESHWATER MOLLUSKS 209

A number of recent studies have attempted A phylogenetic analysis of Unionicola mites to reconstruct evolutionary relationships based on molecular sequence data would among a limited number of mussel-mite taxa undoubtedly be the best approach to resolving based on morphological characteristics (Ed- evolutionary relationships among taxa that wards & Vidrine 2006, Wu et al. 2009) and comprise the genus. There are, however, at molecular data sets (Edwards et al. 2010, Wu et least two compelling reasons why generating al. 2012). The topologies of trees generated by a molecular phylogeny for the group could be these analyses are congruent in that they problematic and thus warrant reconstructing suggest that mites that live in the gills of host the evolution history among these mites based mussels (5 gill mites) are monophyletic. This on morphological data. First, many of the hypothesis is consistent with that of Vidrine et mollusk mites that have been identified and al. (2007) who suggested a shared evolutionary described were collected long ago and would be history among the gill mites based upon difficult to relocate primarily due to host a number of anatomical similarities. These extinction and habitat destruction. Second, studies, however, have revealed conflicting holotypes and representative paratypes of de- hypotheses regarding relationships among Un- scribed species have been preserved in solutions ionicola mites that live in the mantle and foot that have invariably damaged the quality and area of host mussels (5 mantle mites). While integrity of their DNA. In short, a phylogenetic morphologically-based trees recognize mantle analysis of Unionicola mites based on non- mites as a distinct monophyletic grouping molecular data would presumably allow for (Edwards & Vidrine 2006), molecular phylog- greater taxon sampling. enies suggest that these mites are part of Addressing evolutionary relationships among a paraphyletic grade that includes gill mite Unionicola mites based on morphological criteria taxa (Edwards et al. 2010). Thus, although the is not without its challenges, given that so few gill mites represent a monophyletic clade characters historically have been used to di- (Edwards & Vidrine 2006, Vidrine et al. 2007, agnose the genus and its subgenera (Cook 1974). Moreover, a cursory glance at the taxonomic Wu et al. 2009, Edwards et al. 2010), the studies involving Unionicola mites suggests that relationship between gill mites and other a limited number of characters are available for species of Unionicola remains unclear. The phylogenetic inference. Despite the apparent mantle mites appear to be a conglomerate of pitfalls of using morphological data to recon- diverse taxa at the subgeneric level, with some struct the phylogeny of unionicolid mites, Mal- subgenera having morphological affiliations colm Vidrine, a colleague of mine from Louisi- with sponge mites, and others sharing morpho- ana, and I revisited the taxonomic literature for logical similarities with gill mites (Vidrine 1996, the group and generated 158 characters that Edwards et al. 2010). could be used to estimate evolutionary relation- One major caveat of this previous work is ships among most of the currently named that both the morphological and molecular subgenera that comprise the genus, including phylogenetic studies were limited in their geo- relationships between free-swimming taxa and graphical scope (e.g., limited to one continent) those that have adopted symbiotic lifestyles and in their sampling of taxa. Furthermore, the (Edwards & Vidrine 2013). We subsequently trees generated by these studies were based on identified 139 characters that could be used to a relatively small number of characters. For reassess and potentially resolve conflicting hy- example, the morphologically-based phylogeny potheses regarding the phylogeny of Unionicola of Edwards & Vidrine (2006) was constructed mites that occur in association with mollusks using 32 characters. The gene tree generated by (molluscan gill mites and mantle mites). my colleagues and I (Edwards et al., 2010) was A tree based on the Bayesian inference based on 664 bp from the cytochrome oxidase of morphological data for Unionicola mites subunit I gene. Clearly, a more robust phylo- (e.g., representative species from 53 subgenera genetic hypothesis of the genus Unionicola that comprise the genus) is presented in Fig. 2. would require broader taxon sampling (both The Bayesian tree suggests that most of the in terms of geographic distribution and sample free-swimming Unionicola subgenera are a dis- size) and the incorporation of a substantially tinct radiation (see node labeled A). Although larger number of characters into the analysis. the tree recognizes multiple clades of free- 210 PROCEEDINGS OF THE INDIANA ACADEMY OF SCIENCE

Figure 2.—Bayesian tree based on 158 morphological characters for representative species from 53 subgenera of Unionicola mites. Numbers above branches represent posterior probability values. Letters indicate notable clades: A5free-swimming mites; B5Mollusk mites; C5Australian, South American, and North American gill mites; D5mantle mites; E5African, Eurasian, and North American gill mites. Abbreviations in parentheses: FS5free-swimming mites; G5gill mites; M5mantle mites; NA5North America; SA5South America; AFR5Africa; AUSTR5Australia. swimming mites, there appears to be no distinct with molluscan mites. Mollusk mites appear to relationship between the taxa that comprise represent a monophyletic grouping (see node these clades and their geographic distributions. labeled B) and are divided into two major The tree also shows several lineages of clades, with Australian gill mite subgenera free-swimming mites forming a basal grade along with gill mites from South America and EDWARDS—MITES OF FRESHWATER MOLLUSKS 211

North America forming one clade (see node represent the least derived group of gill mites and labeled C) and Unionicola mantle mites (see these mites are the first clade to branch in the node labeled D) and gill mites from Africa, proposed tree for mollusk mite taxa. In the Eurasia, and North America forming the other mollusk mite tree the South American and (see node labeled E). Two species of gill mites North American gill mites form a distinct clade (U. anodontae and U. botswaniana) from the from a monophyletic grouping that includes subgenus Iridinicola appear to be sister taxa to African gill mites and mantle mites. These the mantle mites. This latter group of mites groupings are consistent with the hypothesis appears to represent a more derived lineage that mites on the South American and African within the genus. continents represent early radiations of Union- The tree that resulted from the Bayesian icola from an ancestral stock occurring in phylogenetic analysis of the morphological Australia that occurred in Pangaea prior to its data for Unionicola mollusk mites (e.g., repre- break-up. Mites from the subgenus Unionico- sentative species from 30 subgenera) is pre- lides occur in both the South American and sented in Fig. 3. Based on the typology of this North American continents and their occur- tree, the Australian gill mites are a separate rence in North America appears to represent clade (see node labeled A) from a large mono- a secondary radiation that coincides with the phyletic grouping that includes the world’s diverse radiation of their host mussels on this remaining gill mites along with all of the mantle continent. Mites from the subgenus Prasadatax mites (see node labeled B). Within this larger from India appear to have characteristics that clade, there is a branch that includes gill mites are shared by African gill mites and many of the from North and South America (see node mite subgenera from Eurasia. These African and labeled C). Another well-supported monophy- Eurasian mites occur largely as a distinct clade in letic grouping within the larger mollusk mite the mollusk mite tree. Not surprisingly, three branch is one that is formed by African and subgenera (Dimockatax, Unionicola, and Wol- Laurasian gill mites along with the mantle cottatax) that occur both in Eurasia and North mites (see node labeled D). This mollusk mite America form a monophyletic grouping. Vidrine tree, like the tree generated for Unionicola (1986) has previously argued that mites from subgenera, supports a sister group relationship these North American subgenera represent de- between mantle mites (see node labeled E) and scendant lineages from the Eurasian continent. African and Laurasian gill mites (see node It is important to note that the morphological labeled F). The mollusk mite tree has been trees generated for the Unionicola subgenera and reproduced with the subgeneric designations of the mollusk mites should be viewed as working the species used to generate the tree being hypotheses. We are now in a position to collect shown in parentheses (Edwards & Vidrine sequence data for a broad array of taxa from 2013). With few exceptions, species that have specific regions of these trees to test the validity of been taxonomically assigned to the same sub- the proposed relationships. To this end, an initial genus form distinct clades. first step might be to sample and examine There are some consistencies in the general relationships among the globally distributed, patterns depicted by both the Unionicola and highly speciose, monophyletic clade of mollusk mollusk mite trees. For example, the typologies mites. Future studies could expand on these of these trees suggest that the mollusk mites research findings through a comprehensive as- represent a monophyletic clade. In addition, sessment of the evolutionary history among the they suggest that the mantle mites are a sister closely related Unionicola free-swimming mites. taxon to the African and Eurasian gill mites. A close affinity between mantle mites and gill mites RESOLVING UNIONICOLA PHYLOGENY was also indicated by Edwards et al. (2010) in USING GENOME-LEVEL CHARACTERS their paper assessing evolutionary relationships In an approach that is complementary to among molluscan-mite subgenera of North morphological and sequence-based molecular America. Furthermore, the phylogenetic hy- phylogeny, my lab has begun to sequence the pothesis for the Unionicola mollusk mites, mitochondrial genomes of Unionicola mites in especially the gill mites, appears to dovetail our an effort to assess the potential contributions of present understanding of the diversification of genome-level rearrangements and other unique these mites. The Australian mites are thought to events toward phylogenetic reconstruction 212 PROCEEDINGS OF THE INDIANA ACADEMY OF SCIENCE

Figure 3.—Bayesian tree based on 139 morphological characters for representative species from 30 subgenera of Unionicola mollusk mites. Numbers above branches represent posterior probability values. Letters indicate notable clades: A5Australian gill mites; B5gill mites, excluding those from Australia and mantle mites; C5gill mites from North and South America; D5African and Laurasian gill mites along with the mantle mites; E5mantle mites; F5African and Laurasian gill mites. Abbreviations in parentheses: G5gill mites; M5mantle mites; FS5free-swimming mites; AFR5Africa; AUSTR5Australia; EUR5 Europe; NA5North America; SA5South America. EDWARDS—MITES OF FRESHWATER MOLLUSKS 213

Figure 4.—Comparison of the mitochondrial genome structures of Trombidiformes mites and the horseshoe crab Limulus polyphemus. Green: protein-coding genes, red: tRNA genes, purple: rRNA genes. Circular genome sequences were linearized at the 5’ end of the cox1 gene. Genes transcribed in the same direction as cox1 (left to right) are shown below the line, and genes transcribed in the opposite direction are shown above the line. For protein-coding and rRNA genes, the gene names are shown either in the rectangle or above or below the line. For tRNA genes, gene names are abbreviated with the single-letter abbreviation for the amino acid specified. (Modified from Edwards et al. 2011.) 214 PROCEEDINGS OF THE INDIANA ACADEMY OF SCIENCE among Unionicola mites. As a first step to this years. I am grateful to Malcolm Vidrine, approach, the complete mitochondrial genomes Professor of Biology, Louisiana State Univer- of two species of Unionicola gill mites, Union- sity at Eunice, for his taxonomic expertise icola foili (subgenus Unionicola; Ernsting et al. regarding these mites. As the ancient Chinese 2009) and U. parkeri (subgenus Unionicolides; proverb tells us, ‘‘The beginning of wisdom is Edwards et al. 2011), have been sequenced. The to call things by their right names.’’ I also want annotation of these mitochondrial genomes to thank Brian Ernsting, Professor of Biology, indicated unique gene orders, highly rearranged University of Evansville, for his assistance with in comparison to other Trombidiformes mites molecular protocols and the analysis of molec- (Fig. 4). Moreover, a comparison of the mito- ular sequence data. Finally, I am deeply chondrial genome sequence between U. foili indebted to countless scores of students who and U. parkeri revealed genome-level synapo- dedicated significant portions of their under- morphies, including tRNA rearrangements, graduate lives to work on this obscure group of a significantly longer long noncoding region mites. Much of the research reported in this between tRNAs for U. parkeri, and differences talk was supported by grants from the Indiana in reading frames between species mitochon- Academy of Sciences and UExplore, an un- drial genes (Edwards et al. 2011). Overall, the dergraduate research program at the University differences in genome structure between rela- of Evansville. tively closely-related Unionicola underscore the potential for molecular synapomorphies to be LITERATURE CITED phylogenetically informative within the genus. Baker, R.A. 1976. Tissue damage and leukocytic FUTURE DIRECTIONS infiltration following attachment of the mite Unionicola intermedia to the gills of the bivalve Resolving the evolutionary history of Union- mollusc Anodonta anatina. Journal of Invertebrate icola mollusk mites will provide us with count- Pathology 27:371–376. less avenues for future research. For example, Baker, R.A. 1977. Nutrition of the mite Unionicola a robust phylogeny of Unionicola mollusk mites intermedia Koenike and its relationship to the could be examined in the context of the inflammatory response induced in its molluscan phylogenetic history of their host mussels. A host Anodonta anatina. Parasitology 75:301–308. comparison of the evolutionary relationships Baker, R.A. 1987. Aspects of the life history of between mollusk mites and their host mussels Unionicola ypsilophora (Bonz 1783). Naturalist would present an ideal opportunity to address 112:53–58. not only the degree to which their phylogenies Cook, D.R. 1974. Water Mite Genera and Sub- genera. Memoirs of the American Entomological are congruent, but to understand the mechan- Institute 211–860, Ann Arbor, Michigan. isms responsible for mediating those patterns, Davids, C. 1973. The relations between mites of the including the effects of dispersal capacity by genus Unionicola and the mussels Anodonta and mites (Downes 1989), competitive exclusion Unio. Hydrobiologia 41:37–44. (Davids et al. 1988), and behavioral specificity Davids, C., J. Holtslag & R.V. Dimock, Jr. 1988. (Edwards & Dimock 1995). Also, once general Competitive exclusion, harem behaviour and host patterns of host utilization by symbiotic species specificity of the water mite Unionicola ypsilo- have been elucidated, and the relationship of phora (Hydrachnellae, Acari) inhabiting Anodonta these mites to free-swimming species has been cygnea (Unionidae). Internationale Revue der reconstructed, we can begin to address the gesamten Hydrobiologie 73:651–657. ecological and evolutionary processes respon- Dimock, Jr., R.V. 1983. In defense of the harem: sible for patterns of host association, at both intraspecific aggression by male water mites the regional scale (emphasizing the importance (Acari: Unionicolidae). Annals of the Entomolog- ical Society of America 76: 463–465. of contemporary ecological factors) and over Dimock, Jr., R.V. 1985. Population dynamics of broad geographical areas (emphasizing the Unionicola formosa (Acari: Unionicolidae), a water importance of historical biogeography). mite with a harem. American Midland Naturalist ACKNOWLEDGMENTS 114:168–179. Dimock, Jr., R.V. 1988. Photobiology and behavior There are many people that I would like to of the water mite genus Unionicola: a minireview. thank with regards to my research program Comparative Biochemistry and Physiology involving Unionicola mites over the past twenty 91:193–197. EDWARDS—MITES OF FRESHWATER MOLLUSKS 215

Downes, B.J. 1989. Host specificity, host location tween closely-related Unionicola gill mites. Exper- and dispersal: experimental conclusions from imental and Applied Acarology 54:105–117. freshwater mites (Unionicola spp.) parasitizing Ernsting, B.R., D.D. Edwards, M.F. Vidrine, K.S. unionid mussels. Parasitology 98:189–196. Myers & C.M. Harmon. 2006. Phylogenetic Edwards, D.D. 1988. The population biology of Relationships among species of the subgenus Unionicola formosa from two anodontine mussels Parasitatax (Acari: Unionicolidae: Unionicola) in a North Carolina farm pond. M. S. Thesis. based on DNA sequence of the mitochondrial Wake Forest University, Winston-Salem, North cytochrome oxidase I gene. International Journal Carolina. 72 pp. of Acarology 32:195–202. Edwards, D.D. & R.V. Dimock, Jr. 1991. The Ernsting, B.R., D.D. Edwards, M.F. Vidrine & H. relative importance of size versus territorial Cun. 2008. Genetic differences among sibling residency in intraspecific aggression by symbiotic species of the subgenus Dimockatax (Acari: male water mites (Acari: Unionicolidae). Experi- Unionicolidae: Unionicola): heterogeneity in mental and Applied Acarology 12:61–65. DNA sequence data supports morphological Edwards, D.D. & R.V. Dimock, Jr. 1995. Specificity differentiation. International Journal of Acarol- of the host recognition behavior of larval Union- ogy 34:403–407. icola (Acari: Unionicolidae): the effects of larval Ernsting, B.R., D.D. Edwards, K.J. Aldred, J.S. ontogeny and early larval experience. Fites & C.R. Neff. 2009. Mitochondrial genome Behavior 50:343–352. sequence of Unionicola foili (Acari: Unionicoli- Edwards, D.D. & R.V. Dimock, Jr. 1997. Genetic dae): a unique gene order with implications for differentiation between Unionicola formosa and U. phylogenetic inference. Experimental and Applied foili (Acari: Unionicolidae): cryptic species of mol- Acarology 49:305–316. luscan symbionts. Invertebrate Biology 116:124–133. Fisher, G.R., R.V. Dimock, Jr. & R.E. Kuhn. 2000. The symbiotic water mite Unionicola formosa Edwards, D.D. & M. Labhart. 2000. Genetic (Acari: Unionicolidae) ingests mucus and tissue differences among host-associated populations of of its molluscan host. Journal of Parasitology water mites (Acari: Unionicolidae: Unionicola): 86:1254–1258. allozyme variation supports morphological differ- Hevers, J. 1978. Interspezifische Beziehungen zwischen entiation. Journal of Parasitology 86:1008–1011. Unionicola-Larven (Hydrachnellae, Acari) und Edwards, D.D. & M.F. Vidrine. 2006. Host speci- Chironomidae (Diptera, Insecta). Verhandlungen ficity among Unionicola spp. (Acari: Unionicoli- Gesellschraft fu¨ r Oekologie 7:211–217. dae) parasitizing freshwater mussels. Journal of LaRochelle, P. & R.V. Dimock, Jr. 1981. Behavioral Parasitology 92:977–983. aspects of host recognition by the symbiotic water Edwards, D.D. & M.F. Vidrine. 2013. Mites of mite Unionicola formosa (Acarina, Unionicolidae). Freshwater Mollusks. Malcolm F. Vidrine, Eu- Oecologia 48:257–259. nice, Louisiana. 336 pp. MacArthur, R.D., Jr. 1989. Morphometric and phys- Edwards, D.D., R. Bogardus & N. Wilhite. 1998. iological assessment of the effects of the symbiont, Geographic Differences in Host Specialization Unionicola formosa, on its molluscan host, Andonta between the Symbiotic Water Mites Unionicola cataracta.M.S.Thesis.WakeForestUniversity, formosa and U. foili (Acari: Unionicolidae). Winston-Salem, North Carolina. 72 pp. Pp. 195–206. In Ecology and Evolution of the Mitchell, R. 1955. Anatomy, life history, and Acari. (J. Briun, L. van der Geest and M.W. evolution of the mites parasites fresh-water Sabelis, Eds.), Kluwer Academic Publishers, mussels. Miscellaneous Publications Museum of Dordrecht, The Netherlands. Zoology, University of Michigan No. 89:1–28. Edwards, D.D., D.E. Deatherage & B.R. Ernsting. Mitchell, R. 1965. Population regulation of a water 2004. Random amplified polymorphic DNA mite parasitic on unionid mussels Journal of analysis of kinship within host-associated popula- Parasitology 51:990–996. tions of the symbiotic water mite Unionicola foili Roberts, E., R. Dimock, Jr. & R. Forward, Jr. 1978. (Acari: Unionicolidae). Experimental and Applied Positive and host-induced phototaxis of the Acarology 34:67–77. symbiotic water mite Unionicola formosa. Biolog- Edwards, D.D., M.F. Vidrine & B.R. Ernsting. 2010. ical Bulletin 155:599–607. Phylogenetic relationships among Unionicola Vidrine, M.F. 1986. Five new species in the subgenus (Acari: Unionicolidae) mussel-mites of North Parasitatax (Acari: Unionicolidae: Unionicola)from America based on mitochondrial cytochrome North America and Asia, with a re-evaluation of oxidase I sequences. Zootaxa 2537:47–57. related species. 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Vidrine,M.F.,A.E.Bogan&S.R.Hazelton-Robi- Unionicola formosa. M.A. Thesis, Wake Forest chaux. 2007. Re-evaluation of Australian and South University, Winston-Salem, North Carolina. 43 pp. American Unionicola Haldeman (Acari: Unionicoli- Wu, H., B. Hu, Z. Zhu & C. Wen. 2009. Cladistic dae). International Journal of Acarology 33:49–52. analysis on the genus Unionicola (Acari: Union- Welsh, J. 1930. Reversal of phototrophism in a parasitic icolidae) from China. Entomotaxonomia 31: water mite. Biological Bulletin 59:165–169. 152–160. Welsh, J. 1931. Specific influence of the host on the Wu, H., C. Wen & W. Guo. 2012. Sequence variation light responses of parasitic water mites. Biological of the mitochondrial 12S rRNA gene among Bulletin 61:497–499. Unionicola (Wolcottatax) arcuata (Acari: Union- Werner, W.E. 1983. Discrimination of potential icolidae) from freshwater mussels in China. In- molluscan hosts by the symbiotic water mite ternational Journal of Acarology 38:394–401.

Dale D. Edwards, PhD, 2013-2014 Indiana Academy of Science President. Dale D. Edwards is a professor of biology at the University of Evansville. He earned his B.S. in zoology at Brandon University in Canada, and later completed his M.S. and Ph.D. degrees in biology at Wake Forest University. He is broadly interested in ecology and evolution of organisms with symbiotic lifestyles, and has spent that past 27 years studying the evolutionary ecology of Unionicola mites that live in association with freshwater mussels. His research involving these mites has addressed issues regarding patterns of host specificity, the genetic structure among host-associated populations, patterns of species richness, and the effects that the ectoparasitic larval stages have on their insect hosts, including their potential role in influencing host survival and reproduction. He has also had a keen interest in Unionicola systematics, and has worked in collaboration with Brian Ernsting (University of Evansville) and Malcolm Vidrine (Louisiana State University at Eunice) to address phylogenetic relationships among unionicolid mussel-mites, using both morphological and molecular approaches. He is the author of 25 peer-reviewed scientific publications, and one book titled ‘‘Mites of Freshwater Mollusks.’’