Invertebrates in Endosymbiotic Associations

AMER. ZOOL., 32:557-565 (1992)

Invertebrates in Endosymbiotic Associations'

MARY BETH SAFFO

Institute of Marine Sciences, University of California, Santa Cruz, California 95064

SYNOPSIS. Endosymbiosis is a phenomenon of central importance to thebiology of many invertebrate animals. Parasitic, commensal and mutu-alistic endosymbioses are widely distributed among invertebrate taxa, andhave arguably played a major role in the evolution of several invertebratefamilies, classes and phyla. Sometimes accounting for as much as 50% ofinvertebrate volume or biomass, endosymbionts can profoundly affectthe ecology, physiology, development and behavior of invertebrate hosts.Endosymbiosis raises a number of questions that are worth the serious,sustained attention of a broad range of invertebrate biologists.

INTRODUCTION

Barring the complexities of clonal inver-tebrates, we tend to think of an individualinvertebrate animal as just that: an individ-ual genome, a representative of a singletaxon. But many invertebrate organisms arenot merely individual genomes or singletaxa; as hosts of persistent, intimately asso-ciated endosymbiotic communities, they canalso be viewed as morphological, physio-logical or genetic chimeras of several taxa.With recent research, the pervasiveness andimportance of symbiosis among inverte-brates are beginning to be appreciated, butthey have not yet been integrated intoeveryday teaching and research perspec-tives on general invertebrate biology. Tostimulate such integration, a workshop, TheImpact of Symbiosis on Invertebrate Phys-iology, Ecology, and Evolution, was spon-sored by the Division of Invertebrate Zool-ogy for the Centennial Meeting of theAmerican Society of Zoologists.

DISCUSSION

Symbiotic associations vary in theirselective consequences, in their mode oftransmission, and in their pervasivenessthroughout invertebrate host populations.Endosymbiotic interactions can be harmful(parasitism) to host or endosymbiont; they

1 From the Workshop on The Impact of Symbiosison Invertebrate Physiology, Ecology, and Evolutionpresented at the Centennial Meeting of the AmericanSociety of Zoologists, 27-30 December 1989, at Bos-ton, Massachusetts.

can also be mutually beneficial (mutualism),or have a beneficial effect on one partner,but a negligible effect (commensalism) onthe other. Most commonly, the selectiveeffect on the host or endosymbiont is eithertoo poorly known, or too complex, to definein any of these three simple terms.

Endosymbionts can be intracellular orextracellular inhabitants, transmittedhereditarily (vertically) with their host, ornon-hereditarily (horizontally), necessitat-ing re-establishment of the symbiotic asso-ciation each generation. Some endosym-bionts (as in many parasites) infect onlysome members of a given invertebrate pop-ulation. Others (as in many "mutualistic"or other endosymbioses which apparentlybenefit the host) are chronic symbionts(Saffo, 1991a), inhabiting 100% of the hostpopulation for a significant portion of thehost's life history. Nevertheless, whateverthe exact nature of symbiotic dynamics,endosymbionts can have profound effectson the biochemistry, physiology, morphol-ogy, behavior, population biology, ecologyand evolution of invertebrate hosts. Thisimpact can be demonstrated in a numberof contexts:

• Symbiosis is taxonomically wide-spread among invertebrate animals, involv-ing members of virtually every invertebrateclass and phylum. No invertebrate taxon isentirely symbiont-free. At minimum, at leastsome percentage of individuals in everyinvertebrate species are hosts to parasites,commensalistic symbionts, or to pathogens.

Beyond the ubiquitous distribution of

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558 MARY BETH SAFFO

parasites and pathogens, chronic endosym-bioses (Table 1) are also broadly distributedthroughout invertebrate phyla. Associa-tions between invertebrates and autotro-phic endosymbionts are among the mostwell-known chronic symbioses. For exam-ple, a wide range of fresh-water and marineinvertebrate taxa from temperate and trop-ical latitudes are habitually associated withprotistan or cyanobacterial photoauto-trophs. Chemoautotrophic (especially sul-fur-oxidizing) bacteria are chronic inhabi-tants of vestimentiferan and perviatepogonophorans; lucinids, thyasirids andother bivalves, and several species of nem-atodes, oligochaetes and turbellaria (Ott etal, 1982;Caryera/., 1988; Wood and Kelly,1989).

Many more invertebrate taxa containchronic heterotrophic endosymbionts, mostof which have received little study. Severalspecies of bioluminescent sepioloid squid(Wei and Young, 1989; Mcfall-Ngai andRuby, 1989) harbor luminescent bacteria,as do Pyrosoma (Leisman et al, 1980) andsome insect pathogenic nematodes (Neal-son, 1991). In the above symbioses, at leastone effect of the endosymbionts (biolumi-nescence) is obvious, although the ecologi-cal significance of the luminescence is notalways clear. Less is understood about otherheterotrophic endosymbionts. For instance,although dicyemid "mesozoans" colonizethe kidneys of 100% of the populations oftemperate and boreal octopods, the meta-bolic and ecological impact of the symbiosisis not known (Hochberg, 1983). Heterotro-phic bacteria are found in placozoa (Grell,1981), demosponges and sclerosponges(Vacelet, 1975; Bergquist, 1978); in leechesand earthworms (Buchner, 1965); in thecytoplasm of Nephromyces, a protistanendosymbiont of molgulid ascidians (Saffo,1990, 1991a); in shipworms and terrestrialprosobranchs {Pomatias elegans: Buchner,1965); and in species of echinoids, brittlestars and asteroids (De Ridder et al, 1985;Walker and Lesser, 1989; Bosch, 1992).Mollicutes (mycoplasmas) and walled bac-teria have been reported from larval andadult bryozoans (Lutaud, 1969; Woollacott,1981; Zimmer and Woollacott, 1983; Boyleet al., 1987). Ten percent of all insect species

(Douglas, 1989; Ishikawa, 1989), as well assome arachnids {e.g., ticks and mites), har-bor non-pathological bacterial endosym-bionts, either as extracellular intestinalsymbionts (as in termites and cockroaches),or as intracellular inhabitants of "myce-tomes" or other organs (as in grain weevils,aphids, sucking lice, and cockroaches). Onlyin shipworms (Waterbury et al., 1983),luminescent symbioses and herbivorousinsects have the metabolic activities of het-erotrophic symbiotic prokaryotes beenclearly demonstrated.

• Especially among chronic endosym-bioses, a significant percentage of "inver-tebrate" biomass can be microbial symbi-ont biomass. A typical termite gut, forinstance, contains as many as 107 protozoancells and lO9"10 bacterial cells (Smith andDouglas, 1987), accounting for 33-50% oftotal termite weight (Whitfield, 1979). Sim-ilarly, bacterial symbionts make up 37.5%of the uncontracted mesohyl volume of thedemosponge Verongia, equal to, or slightlyexceeding, the volume of host cells (Vacelet,1975; Bergquist, 1978). In larvae of the grainweevil Sitophilus oryzae, there are 1 to 3million endosymbiotic bacteria, compara-ble to the total number of host cells (Nardonand Grenier, 1991). Parasitic symbionts{e.g., rhizocephalan symbionts in crabs,acanthocephalan symbionts in pill bugs) canalso take up a significant percentage of hostvolume (Moore, 1984a, b\ Schmidt andRoberts, 1989).

• Endosymbiosis has played a major rolein the evolution of several invertebrate taxa.The ubiquitous distribution of endosym-bionts among several groups of inverte-brates suggests that chronic symbionts havebeen intimately involved in the evolutionand radiation of a number of invertebrategenera, families and orders (lucinid bivalves,molgulid ascidians, hermatypic scleractin-ian corals: Saffo, 1991a, b), classes (Hiru-dinea: Buchner, 1965) and even phyla(Pogonophora: Vetter, 1991). Endosym-bionts can affect the evolution of their hostsdirectly, by coevolution or cospeciation withtheir hosts, or indirectly, by their impact onhost metabolism and ecology.

Many invertebrates are themselves sym-bionts. Several orders and classes, especially

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ENDOSYMBIOSES IN INVERTEBRATES 559

among flatworms, nematodes, and annelids,consist exclusively of endo- or ecto-para-sites, and some phyla (orthonectids,dicyemids and acanthocephalans) containonly endosymbiotic species. Several otherorders and classes (e.g., polychaetes, iso-pods, copepods, cirripedes), include manyparasitic or commensalistic members. Theseorganisms show striking morphological,developmental and physiological adapta-tions to endosymbiotic life.

Endosymbiont-induced speciation hasbeen demonstrated, thus far, in about adozen species of arthropods (Thompson,1987; Nardon and Grenier, 1991). Patho-logic or nonpathologic symbionts can effecthost speciation either through reproductiveisolation of individuals with differing (orabsent) endosymbiotic communities, orthrough divergent selection of host popu-lations which differ in symbiont composi-tion or in dynamics of host-symbiont inter-actions (Thompson, 1987;Saffo, 19916).

• Invertebrate endosymbioses can havemajor ecological impact, both on the habitatrange and inter-species relationships of theinvertebrate hosts themselves, and on theecosystems of which they are a part.

Many invertebrate hosts of chronic endo-symbioses, such as termites, cockroaches,scleractinian corals, and molgulid ascidiansare abundant or globally distributed taxa,conspicuously present in terrestrial ormarine ecosystems. For these and othersymbiotic invertebrates, the physiologicalcontributions of chronic endosymbionts canallow exploitation of profoundly new niches.Symbioses with autotrophic symbionts haveallowed species from at least 7 phyla (Table1) to lead partially or exclusively autotro-phic lives, where some of them, such asscleractinian corals, Pogonophora, andlucinid bivalves, play significant or even keyroles in tropical reefs, sulfur-rich habitatsand other marine communities. The met-abolic contributions of cellulases, aminoacids, B vitamins, sterols, and nitrogen fix-ation or nitrogen recycling by intracellularbacteria and microbial intestinal symbiontshave allowed insects, bivalves and others toexploit specialized, nutritionally limitedplant diets such as wood, phloem, and grain.All blood-sucking invertebrates, including

sucking lice, leeches and ticks, are obligatelyassociated with bacterial endosymbionts.

• Beyond the contributions of symbiontsto host nutrition per se, both parasitic andmutualistic endosymbioses can have pro-found effects on many other aspects of thebiology of invertebrate hosts. In severalmutualistic endosymbioses, some of theseeffects can be interpreted nevertheless asgeneral consequences of symbiont contri-butions to host nutrition, underscoring theimpact of endosymbiont metabolism inmany such symbioses. In bacterial-grainweevil symbioses, for instance, aposym-biotic populations of the hosts, Sitophilusoryzae and S. zeamais (Nardon and Gren-ier, 1991) cannot fly. Further, the devel-opment time of aposymbiotic weevils islengthened, and their fertility reduced, com-pared to their symbiotic counterparts. Allthese effects are plausibly linked to the con-tributions of vitamins and amino acids andenhancement of mitochondrial enzymeactivity by the bacterial symbionts of Si-tophilus.

Other effects of symbiont infection sug-gest biochemical interactions that are nottied to nutrient exchange between symbiontand host. In rhizocephalan-parasitized crus-taceans, for instance, the alteration of sec-ondary sexual characteristics of hosts, andreduction or elimination of host reproduc-tion by parasites result from hormonalinteractions between parasite and host. Inseveral insects and mites, bacterial or pro-tozoan symbionts can alter sex ratios of hostpopulations, usually through selective mor-tality of male embryos or juveniles (Hugeret al, 1985).

Parasites can also dramatically alter hostbehavior, especially that of invertebrateintermediate hosts. Acanthocephalan infes-tation of arthropods (Moore, 1984a, b) canreverse typical host responses to light (ininfected amphipods and cockroaches),humidity, shelter and background color(infected pill bugs). Individuals of the gas-tropod Ilyanassa obtusata parasitized by thetrematode Gynaecotyla adunca crawl higherup into the intertidal zone than eitherunparasitized individuals, or individualsparasitized by other species (Curtis, 1987);G. adunca and other trematode species

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TABLE 1. Chronic endosymbioses among invertebrates.

Host phylum

Placozoa

Sponges

Cnidaria

Platyhelminthes

Nematoda

Annelids

Pogonophora

Class

Demospongiae

DemospongiaeDemospongiae

and Sclerospon-

giaDemospongiae

and Calcarea

hydrozoa

hydrozoa

scyphozoa

anthozoa

turbellaria

hirudinea

oligochaetes

perviata and vesti-mentifera

Example

Trichoplax ad-haerens

Cliona

SpongillaVerongia, Cerato-

porella

about 38 genera

Chlorohydra

Velella, Millepora

Mastigias, Cassio-peia

scleractinian cor-als

acoels

Paracatenula spp.neorhabdocoelsAstomonema jen-

neriXenorhabdus spp.

Placobdella, ich-thyobdellids

Hirudo medicina-lis

Phallodrilus leuko-dermata

lumbricids

Symbiont

bacteria

Symbiodinium

Chlorellaheterotrophic bac-

teria

cyanobacteria

Chlorella

dinoflagellates

dinoflagellates

dinoflagellates

prasinophytes, dino-flagellates, diatoms

bacteriaChlorellabacteria

luminescent bacte-ria

bacteria

1. Pseudomonas2. bacteria

bacteria

bacteria

sulfur-oxidizingbacteria

Symb. locale

fiber cells: cister-nae of E.R.

mesohyl

mesohyl

gastrodermal cells

gastrodermal cells

gastrodermal cells

gastrodermal cells

host vacuoles nearbody wall

mesenchymegut rudiment

intestine/vesicles

esophageal ceca

1. intestinallumen

2. urinarybladder

nephridial ampul-

trophosome

Symbiont activity*

?

photoautotroph

photoautotroph?some facultative

anaerobes

photoautotroph+(?) nitrogenfixation

photoautotroph

photoautotroph

photoautotroph

photoautotroph

photoautotroph

chemoautotrophphotoautotrophchemoautotroph

entomopatho-genesis of host

suppl. nut.

1. blood feeder:suppl. nut.

2. ?

chemoautotroph

?

chemoautotroph

Reference

Grell, 1981; Grelland Benwitz,1981

Smith and Douglas,1987

Bergquist, 1978Vacelet, 1975; San-

tavy et al., 1990

Wilkinson, 1983;Smith and Doug-las, 1987






Oltet al., 1982Douglas, 1987Ottet al., 1982

Nealson, 1991

Buchner, 1965

Buchner, 1965

Giere, 1981; Fel-beck etal., 1983

Buchner, 1965


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TABLE 1. Continued.

Host phylum

Mollusca

Echiura

Bryozoa

Echinodermata

Chordata(urochordates)

Class

gastropods

bivalves

cephalopods

echinoids

asteroids

ophiuroids

ascidiacea

Example

sacoglossans, nu-dibranchs

terrestrial proso-branchs

lucinids, thyasi-rids, Calypto-

Tridacna

shipworms

temperate/borealoctopods

Euprymna sco-lopes

Bonnellia

Watersipora

Bugula spp.

Echinocardium

Luidia

Amphipholis squa-mala

tropical didemnids

Symbiont

(chloropalsts)

bacteria

bacteria

dinoflagellates

bacteria

dicyemids

bacteria

1. cyanobacteria2. heterotrophic

bacteriamollicutes (myco-

plasmas)

bacteria

bacteria

bacteria

bacteria

cyanobacteria (in-cluding prochlo-rophytes)

Symb. locale

gut or digestive di-verticula

"concrementgland"

gills

siphonal tissue

gills

renal sac

epithelial light or-gan

visceral coelom

pallial sinus (lar-vae); funicularbodies (adults)

intestinal cecum

extracellular; sub-cuticular regionnear gut

bursae and devel-oping embryos

atrial cavity

Symbiont activity*

(photoautotroph)

urate recycling?

chemoautotroph,methanotroph

photoautotroph

cellulase, nitrogenfixation

?

bioluminescence

1. N fixation?2. ?

?

sediment process-ing?

?

embryo growthand develop-ment?

photoautotrophyand N fixation

Reference


Buchner, 1965

Wood and Kelly,1989

Smith and Douglas,1 0871 7O /

Waterbury el al.,1983

Hochberg, 1983

Wei and Young,1989; McFall-Ngai and Mont-gomery, 1990


Zimmer and Wool-lacott, 1983;Boyle el al, 1987

Lutaud, 1969;Woollacott, 1981

De Ridder et al,1985

Bosch, 1992

Walker and Lesser,1989


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TABLE 1. Continued.

Host phylum

Arthropoda(partial list)

Class

thaliacea

arachnida

insecta

Example

molgulids

Pyrosoma

gamasid mites (Li-ponyssus)

ixodids and arga-sids

Cryptoceros

Periplaneta ameri-cana

scale insects

aphids e.g., Eusce-

bed bugs (e.g., Ci-mex)

sucking lice, e.g.,Pediculus hu-manus

tephritid fruit flies

Culex, AedesDrosophila spp.

screwworm Cochli-omyia homini-vorax

tsetse flies (Glossi-na)

cranefly larvae

Symbiont

Nephromyces(with intracellu-lar bacteria)

bacteria

bacteria

rickettsiae

protozoa

bacteria

bacteria

bacteria

bacteria

bacteria

bacteria

Wolbachiamycoplasmas, spi-

roplasmas, rick-ettsias, viruses

bacteria (Providen-cia rettgeri)

bacteria

bacteria

Symb. locale

renal sac

intracellular

mycetocytes nearintestine

Malpighian tu-bules, ovaries

hindgut

1. hindgut2. fat body

mycetocytes

mycetome

midgut

mycetocytes nearmidgut wall

midgut cecum(larva); esopha-geal pouch andhindgut (adults)

egg, germ cellsvarious tissues,

hemolymph

midgut

hindgut

Symbiont activity*

urate catabolism

bioluminescence

blood feeders:suppl. nut.


cellulase

1. cellulase,suppl. nut.?

2. uraterecycling?

xylem and phloemfeeders: suppl.nut.

B vitamins, sterols


blood feeders: Bvitamins

suppl. nut.?

?7

7

blood feeders: Bvitamins

cellulase

Reference

Saffo, 1990, 1991a

Leisman el ai,1980

Buchner, 1965

Buchner, 1965;Hayes and Burg-dorfer, 1989

Smith and Douglas,IQS71 7O '


Tremblay, 1989

Douglas, 1989

Douglas, 1989

Douglas, 1989

Buchner, 1965;Smith and Doug-las, 1987; Gass-ner, 1989

Gassner, 1989Thompson, 1987;

Gassner, 1989

Gassner, 1989

Douglas, 1989


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influence, both positively and negatively(depending on the species), the response ofnonbreeding /. obsoleta to carrion (Curtis,1985). As Moore (19846) noted, field obser-vations of invertebrate behavior need to takeinto account that some observed behaviors"may have been 'rigged' " by the presenceof endoparasites.

In some cases {e.g., the symbiotic lightorgans of sepiolid squid, colonized by Vib-rio fischeri: McFall-Ngai and Ruby, 1991)the development of symbiont-containinginvertebrate organs is affected by the pres-ence or absence of symbionts. In others, theabsence of chronic symbionts may affect notonly the development of the symbioticorgan, but larger developmental patterns:Schwemmler (1989) has asserted, though notwithout controversy (Douglas, 1989), thataposymbiotic leafhoppers do not developabdomens. In addition, the function andevolution of several other invertebratestructures (e.g., mycetocyte tissues of otherinsects, the renal sac of molgulid ascidians,the trophosome of pogonophorans) areclosely tied to the chronic presence ofmicrobial symbionts in such tissues.

Given such data, it is clear that symbioticinvertebrates are not marginal exotica, butrather a significant phenomenon of inver-tebrate biology worthy of the serious, sus-tained attention of a broad range ofresearchers. From this perspective, work-shop participants have exploited novelexperimental approaches and less familiarinvertebrate systems to provoke fresh viewson several symbiotic questions:

• (Mark Patterson) How is the metaboliceconomy of endosymbionts affected by theirlack of direct communication with the out-side environment? How does the architec-ture of the host-environment interface affectnutrient and oxygen flux in the endosym-biont?

• (Wayne Sousa) What factors determinethe diversity and density of symbiotic com-munities within an invertebrate host? Whatrole do interspecific interactions, such ascompetition, play in structuring commu-nities of endoparasites?

• (Michael M. Martin) How do mutu-alistic endosymbioses evolve? How does

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564 MARY BETH SAFFO

mutualism and endosymbiosis affect pat-terns of speciation in symbiotic partners?

The following articles document the par-ticipants' perspectives on these questions,drawn from their studies of symbioticinvertebrates in marine and terrestrial hab-itats. While focused on particular cases ofsymbiotic interactions—biomechanicalaspects of algal-cnidarian symbiosis, thecommunity ecology of trematode parasitesin marine gastropod hosts, and the evolu-tion of insect-fungus symbioses—we hopethat the questions raised by the workshopwill play a broader role in helping restruc-ture our general perspectives both on sym-biosis and on invertebrate biology.

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Invertebrates in Endosymbiotic Associations