Evolution of host- and habitat association in the wood-feeding cockroach, Cryptocercus

*Corresponding author. E-mail: [email protected]

Biological Journal of the Linnean Society, 2002, 75, 163–172. With 5 figures

INTRODUCTION

Members of the cockroach genus Cryptocercus Scudder(Dictyoptera: Cryptocercidae) are wood-feeding, sub-social insects that inhabit temperate forests of thePalaearctic and Nearctic (Cleveland et al., 1934; Clarket al., 2001). Two species of Cryptocercus occur in thePalaearctic: one in eastern Russia (Cryptocercus relic-tus Bei-Bienko) and one in south-western China(Cryptocercus primarius Bei-Bienko). All five Nearcticspecies occur in the USA: Cryptocercus clevelandiByers in the Coastal and Cascade Mountains of north-ern California and south-western Oregon; Cryptocer-cus darwini Burnside et al. Cryptocercus garciaiBurnside et al. Cryptocercus punctulatus Burnsideet al. and Cryptocercus wrighti Burnside et al. in statesalong the Appalachian and Allegheny Mountains.

Genetic variation within and among the Nearcticand Palaearctic species of Cryptocercus has beeninvestigated extensively, including chromosomenumber variation (Kambhampati et al., 1996; Luykx,1983), variation in DNA sequence of the mitochondr-ial ribosomal RNA genes (Kambhampati et al., 1996;Burnside et al., 1999; Steinmiller, Kambhampati &Brock, 2001), variation in nuclear ribosomal RNAgenes and internal transcribed spacer (Hossain &Kambhampati, 2001), and variation in ribosomal RNAgenes of endosymbionts harboured by Cryptocercus(Clark et al., 2001). All of the above studies foundextensive genetic variation among the various Cryp-tocercus species, suggesting that they diverged tens ofmillions of years ago.

Given the extensive genetic divergence and disjunctgeographical distribution, our objective was to deter-mine if Cryptocercus species have also diverged in ecological characters. Specifically, we wished to

© 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 75, 163–172 163

Evolution of host- and habitat association in the wood-feeding cockroach, Cryptocercus

SRINIVAS KAMBHAMPATI1*, JEFFREY W. CLARK1 and BRENT L. BROCK2

1 Department of Entomology, Kansas State University, Manhattan, KS 66506, USA2 Division of Biology, Kansas State University, Manhattan, KS 66506, USA

Received 11 April 2001; accepted for publication 19 July 2001

Members of the cockroach genus Cryptocercus are subsocial insects that live in temperate forests and feed on decom-posing logs. At present, seven species are recognized worldwide: four in the eastern USA, one in the western USA,and one each in Russia and China. Genetic variation within and among the Nearctic species has been character-ized extensively in previous studies. However, whether there has been a corresponding divergence in the host andhabitat association of Cryptocercus species is not known. Here, we report on differences in host and habitat asso-ciation among six of the seven Cryptocercus species, estimated from field observations, elevation data, and landcover data. Our results indicated that the eastern and western USA species differ from one another in their dis-tribution patterns, abundance, and habitat association. The eastern USA species are associated largely with decid-uous forests, whereas the western USA and the Russian species are associated with evergreen forests. Thus, theeastern USA species, which are evolutionarily the most recent ones, have adapted to a different set of tree speciesrelative to the basal species. There were also differences in the habitat association of the various species. Specifi-cally, in the eastern USA, Cryptocercus darwini, evolutionarily the most recent species, occupied a habitat that ispredominantly at low elevation [<400m above sea level (ASL)] while all the other Nearctic species and the Russianspecies occupied a habitat that is at relatively higher elevations (>400m ASL). Mapping of the above traits on aphylogenetic tree revealed that the evolutionary trend in Cryptocercus with regard to host and habitat associationhas been toward the utilization of low elevation habitats dominated by deciduous forests. © 2002 The LinneanSociety of London, Biological Journal of the Linnean Society, 2002, 75, 163–172.

ADDITIONAL KEYWORDS: cockroach – habitat association – geographical information system – phylogeny.

determine if the species differed in their host andhabitat association and, if so, whether there is a dis-cernable evolutionary trend in those traits. This issueis relevant because, despite much recent debate on theevolution and taxonomy of Cryptocercus (Thorne &Carpenter, 1992; Grandcolas, 1994, 1999; Kambham-pati et al., 1996; Nalepa et al., 1997; Burnside et al.,1999; Nalepa & Bandi, 1999; Lo et al., 2000), few com-parative studies have been done on the natural historyof Cryptocercus, and little is known about interspecificdifferences in habitat use and association. The implicitassumption in many studies has been that all Crypto-cercus species are similar in their biology, habitat use,and host association. All species in the genus havebeen labelled ‘generalists’ with regard to habitat andhost association, and have been assumed to have lowvagility due to their apterous nature according tostudies of only the eastern USA species or scant evi-dence (Cleveland et al., 1934; Mamaev, 1973; Grand-colas, 1994, 1999; Nalepa et al., 1997; Nalepa & Bandi,1999). Moreover, there appears to be little morpholog-ical divergence among the various species (Burnsideet al., 1999; Nalepa et al., 1997).

In this paper, we compare and contrast the host andhabitat association of six of the seven Cryptocercusspecies based on field observations, geographical infor-mation system (GIS) data, and published studies. TheGIS is a computer-based information source that facil-itates the use of geographically referenced data forvarious purposes. During the past few years, GIS hasbecome a widely used tool in a variety of disciplines(Kidd & Ritchie, 2000). Within the life sciences, GIShas been used for studies of biodiversity (Jones et al.,1997), distribution mapping (Lehmann, Jaquet &Lachavanne, 1994), prediction of future distributions(Walker, 1990), and population viability (Lindenmayer& Possingham, 1995). However, despite its tremen-dous potential, GIS has rarely been used for evolu-tionary studies (Kidd & Ritchie, 2000). We describe anovel use for GIS: characterizing and comparing thelarge scale features of the habitat occupied by a set ofclosely related species and combining them with phy-logenetic information to detect changes and trendsover evolutionary time in habitat association. Specifi-cally, we report on differences among Cryptocercusspecies in their relative densities and distribution pat-terns, the vegetational composition of the habitat theyoccupy, and the elevational profile of the area in which

they are distributed. By mapping the habitat and hostassociation on a phylogenetic tree, we show that thereis a discernable trend in the evolution of host andhabitat association of Cryptocercus species.

The GIS data and the approach we adopted providedinformation that is qualitatively and quantitativelydifferent from that derived solely from field observa-tions. That is, the approach we took allows for a largescale characterization of the habitat occupied by anorganism that is not possible based on field obser-vations alone. Furthermore, because we could notsample every location in which the cockroaches areexpected to occur, the field observational data fromeach individual site do not necessarily reflect thecharacteristics of the entire habitat. Finally, it wouldbe difficult, if not impossible, to quantify the relativeproportions of the different types of forest and the ele-vational profile of the habitat from field observationsalone. However, field observations can provide specificinformation, such as the presence of particular treespecies, that can not be obtained by a large scale char-acterization of the habitat by GIS.

MATERIAL AND METHODS

Two approaches were taken to characterize the habitatof Cryptocercus in the USA. First, field observationson the distribution and habitat of the eastern specieswere made during May 1999, and those on C. cleve-landi, in the western USA, during August 1999. Forty-eight sites in the eastern USA and 36 in the westernUSA, encompassing the known distribution of Crypto-cercus, were surveyed (Fig. 1). The sites were selectedby looking for fallen logs in forested areas. Decayinglogs of various sizes and belonging to several treespecies were split open with an axe and Cryptocercusindividuals, if present, were collected and preserved in80% ethanol. Three to 10 logs were examined at eachof the 84 sites. If well-tunneled logs and/or frass, butno cockroaches, were found in the initial two-to-threelogs, an extensive localized search was initiated andup to eight additional logs were examined. If no cock-roaches were found after intense examination thesearch was terminated and notes were taken on thepresence/absence of galleries and/or frass within theexamined logs. At all sites observations on canopystructure and floral composition, as well as understorystructure and composition, were recorded. In addition,

164 S. KAMBHAMPATI ET AL.

© 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 75, 163–172

Figure 1. (A) Sampling sites for the four Cryptocercus species in the eastern USA. The symbols (in white) represent thefour species as follows: square, C. darwini; triangle, C. garciai; pentagon, C. punctulatus; circle, C. wrighti. The solid blackcircles are sampling locations in which no specimens were found. The sites enclosed by the box shown in panel B. (B) Aclose-up of sampling sites for Cryptocercus species in south-western North Carolina and north-eastern Georgia. Symbolsfor species as above. (C) Sampling sites for C. clevelandi in the western USA.

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HABITAT USE BY CRYPTOCERCUS 165


A

B

C

estimates of latitude, longitude, and elevation weremade at each site using a hand-held GPS unit. Noteswere taken on the relative density of cockroaches ateach site in which they were found.

No diagnostic morphological characters have yetbeen identified for the Nearctic species; however, eachspecies is characterized by a unique mitochondrialDNA haplotype, discernable by the sequence of the two ribosomal RNA genes (Burnside et al., 1999; Steinmiller et al., 2001). Therefore, DNA sequence of portions of the 12S rRNA and 16S rRNA genes (seeBurnside et al., 1999 for details) was obtained from asubsample of the specimens collected at each site toidentify them to species. The details of the distributionwere provided by Steinmiller et al. (2001).

The second approach involved the use of GIS datarelevant to the distribution of Cryptocercus species inthe USA. Specifically, the habitat of the five Crypto-cercus species in the context of elevation and vegeta-tion cover was analysed using Arc/Info GIS (ESRI,Redlands, CA). Species ranges were estimated by cal-culating minimum convex polygons (MCP) or a kernelestimate (see below) for each species from field sam-pling locations. A MCP is the smallest polygon com-posed only of convex sides needed to encompass allpoints within the distribution of a species (Worton,1987). Elevation data within the species range wereobtained from the US Geological Survey GTOPO30data containing elevations at 30 arc-second (ª 1 km)intervals. These data were reclassified to producedigital elevation models (DEM) containing five eleva-tion classes [in meters above sea level (ASL)]: 1–397,398–793, 794–1189, 1190–1585, and 1586–1981. Veg-etation cover data were obtained from the US Geo-logical Survey/US Environmental Protection AgencyNational Land Cover Data (NLCD). The NLCDcontain vegetation classification at 30 ¥ 30m pixelresolution derived from Landsat imagery. All GISlayers were projected to Albers Conformal Conic(datum = NAD83, spheroid = GRS80). The MCP foreach of the five species was superimposed with eleva-tion and vegetation layers to estimate the percentagearea occupied by each elevation or vegetation classwithin a species’ range. For vegetation analysis, only deciduous forest, evergreen forest, and mixedforest classes were included because these were theonly land cover types relevant to Cryptocercusdistribution.

The habitat, as defined above, was also character-ized using a kernel method (Worton, 1989). In thismethod, the animal’s position in a plane is estimatedfrom a random sample of locational observations madeon an animal in its home range. A major advantage ofthe kernel methods is that they free the estimatesfrom parametric assumptions and have well-under-stood, consistent statistical properties (Worton, 1989).

We utilized the program Kernel Home Range (KHR)which is a part of Animal Movement, an ArcViewextension (Hooge & Eichenlaub, 1997). It calculates afixed kernel home range utilization distribution(Worton, 1989) as a grid coverage using either ad hoccalculation of a smoothing parameter (used in thisstudy), least squares cross validation (Silverman,1986), or a user input for the smoothing parameter, H. The bivariate normal density kernel was used assuggested by Worton (1989).

To allow for comparison of the Nearctic with thePalaearctic species, a literature search was under-taken for any published data on the habitat and dis-tribution of C. relictus and C. primarius. Virtually noinformation was available for C. primarius other thanthe fact that specimens have been collected in twolocations in Sichuan province of China (Bei-Bienko,1935). For C. relictus, an account of its host andhabitat association (Mamaev, 1973) and the elevationsof three locations (Bei-Bienko, 1935; Asahina, 1991)have been published.

Phylogenetic relationship among the six Cryptocer-cus species (five from the USA and C. relictus) was pre-viously inferred based on DNA sequence of nuclearand mitochondrial genes of Cryptocercus and genes oftheir endosymbionts (Burnside et al., 1999; Clarket al., 2001; Hossain & Kambhampati, 2001; Stein-miller et al., 2001). Specifically, the phylogenetic infer-ence was based on portions of the mitochondrial 12SrRNA and 16S rRNA genes, portions of the nuclear5.8S rRNA and 28S rRNA genes, and the entirenuclear internal transcribed spacer 2 of Cryptocercus,as well as portions of the 16S rRNA and 23S rRNAgenes from the endosymbiont, Blattabacteriumcuenoti, harboured by Cryptocercus. The DNA se-quences, after alignment, yielded 3840 characters.Parsimony analysis yielded a single tree, which wasused in this study to examine the trends in host andhabitat association of Cryptocercus over evolutionarytime. Complete details of the phylogenetic analysiswere given by Clark et al. (2001).

RESULTS AND DISCUSSION

DISTRIBUTION PATTERNS

Forty-eight sites were sampled in the AppalachianMountains, 38 of which yielded Cryptocercus (Fig. 1).In eight sites in north-eastern Kentucky and one siteeach in Georgia and North Carolina, no cockroachesor signs of their presence (e.g. galleries, frass) werefound despite the presence of what appeared to behabitat that Cryptocercus occupy in other parts of theAppalachian Mountains. With the exceptions notedabove, the four Appalachian Cryptocercus species collectively exhibited a near-continuous, north–south



distribution from north-western Virginia to north-eastern Alabama.

Relative to the eastern USA species, the distributionof C. clevelandi was fragmented and patchy. Of the 36sites that were sampled throughout northern Califor-nia and western Oregon, only 12 yielded specimens(Fig. 1). In a majority of the sites in which cockroacheswere found, many logs had to be opened and examined

before any specimens were located, indicating that thepopulation density of C. clevelandi in general is low,relative to the Appalachian species.

HOST ASSOCIATION

Among the most common tree species found in theAppalachian sampling sites were tulip poplar (Lirio-



1

2

3

4

1

1

1

2

3 3

4

Figure 2. (A) The vegetational and elevational profile of Cryptocercus habitat in the eastern USA and the minimum convexpolygons used to quantify the habitat of the four species. (B) The vegetational and elevational profile of Cryptocercushabitat in the eastern USA and the kernels used to quantify the habitat of the four species. The numbers represent thefour species as follows: 1, C. darwini; 2, C. garciai; 3, C. wrighti; 4, C. Punctulatus.

A

B

dendron tulipifera), mountain magnolia (Magnoliafraseri), umbrella tree (Magnolia tripetala), white pine(Pinus strobus), Fraser fir (Abies fraseri), and severalspecies of birch, beech, ash, hickory, oak, and maple(Betula, Fagus, Fraxinus, Carya, Quercus, and Acerspecies, respectively). In addition, we also noted thepresence of dogwood (Cornus sp.), Virginia pine (Pinusvirginiana), eastern hemlock (Tsuga canadensis), andsycamore (Platanus sp.).

In contrast to the Appalachian species, C. clevelandiwas found almost exclusively in sites where Douglasfir, Pseudotsuga taxifolia, was the dominant treespecies along with the presence of big cone Douglas fir(Pseudotsuga glaucus) and alpine fir (Abies lasio-carpa). The presence of the following additional treespecies was noted: Ponderosa pine (Pinus ponderosa),silver fir (Abies alba), redwood (Sequoia sempervirens),vine maple (Acer circinatum), willow (Salix spp.),white oak (Quercus alba), and western white pine(Pinus monticola).

The land cover data for the area occupied by each ofthe five Nearctic Cryptocercus species are shown inFigures 2–4. Both the MCP and the kernel estimates(Figs 2, 3) indicated that ª 82% of the area occupied

by C. clevelandi is composed of evergreen forests, 2%of deciduous forests, and 16% of mixed forests (Fig. 4).In contrast, the area occupied by each of the fourAppalachian species was dominated by deciduoustrees and consisted of ª 51–84% deciduous forest,4–20% evergreen forest, and 11–29% mixed forest(Fig. 4). Published information (Mamaev, 1973) indi-cated that C. relictus occurs in forests dominated byKorean fir (Abies koreana) and Korean pine (Pinuskoraiensis), which are a part of the ‘relict forest’formed during the Tertiary and are remnants of theArcto-Tertiary flora.

ELEVATIONAL PROFILE

The elevational profile of the area occupied by each of the five Nearctic species is summarized inFigures 2–4. A vast majority (>90%) of the area occu-pied by the four Appalachian species was within the first three elevational classes, i.e. between 1 and1189m ASL (Fig. 4). However, while >80% of the areaoccupied by C. wrighti, C. punctulatus, and C. garciaiwas between 398 and 1189m ASL, ª 55% of the areaoccupied by C. darwini was <397m ASL and only



Figure 3. (A) The vegetational and elevational profile of C. clevelandi habitat in the western USA and the minimumconvex polygons used to quantify the habitat. (B) The vegetational and elevational profile of C. clevelandi habitat in thewestern USA and the kernels used to quantify the habitat.

A B

ª 35% between 398 and 793m ASL (Fig. 4), indicatingthat C. darwini occurs in a low-elevation habitat, rela-tive to the other three Appalachian species. In thewestern USA, ª 80% of the area occupied by C. cleve-landi was between 398 and 1189m ASL (Fig. 4) andin this regard C. clevelandi was similar to C. wrighti,C. punctulatus, and C. garciai. Extensive data are not available for the elevational profile of C. relictushabitat; however, existing records—2040 and 4270mASL (Bei-Bienko, 1935) and 1000m ASL (Asahina,1991)—indicate that it likely occurs at higher elevations.

The vegetational and elevational characteristics of the habitat, whether quantified using the MCPmethod or the Kernel method, were highly similar(Fig. 4). The only substantive difference was in the ele-vational profile of the habitat occupied by C. garciai.

When estimated using the MCP method, ª 8% of thearea occupied by C. garciai was < 397m ASL, whereaswith the kernel method ª 32% of the area occupied bythe above species was <397m ASL. Both methods,however, indicated that a majority of the area occu-pied by C. garciai is above 398m ASL.

EVOLUTIONARY TRENDS

Previous phylogenetic studies (Kambhampati et al.,1996; Burnside et al., 1999; Clark et al., 2001; Stein-miller et al., 2001) have indicated that C. clevelandi isthe basal species in the Nearctic and the two oldestAppalachian species are C. wrighti and C. punctula-tus. In addition, the Russian C. relictus is basal to theNearctic species complex (Clark et al., 2001). It hasbeen estimated (Clark et al., 2001) that the ancestors



Figure 4. Bar graphs showing the characteristics of the habitat occupied by the five Nearctic Cryptocercus. (A) The rela-tive proportions of the different types of land cover in areas occupied by the various Cryptocercus species as determinedby the minimum convex polygon method. (B) The relative proportions of the different types of land cover in areas occu-pied by the various Cryptocercus species as determined by the kernel method. In both cases, ‘mixed’ refers to forests inwhich neither evergreen nor deciduous trees compose >75% of the area. (C) The elevational profile of the area occupied bythe five Cryptocercus species in the USA as determined by the minimum convex polygon method. (D) The elevational profileof the area occupied by the five Cryptocercus species in the USA as determined by the kernel method.

of present-day Appalachian species diverged from the ancestors of C. clevelandi at least 53–88 millionyears ago; C. punctulatus and C. wrighti diverged fromeach other >23–38 million years ago and C. darwiniand C. garciai, >13–20 million years ago. All of theabove are minimal values because they are based on divergences between genes of endosymbionts, B.cuenoti, harboured by Cryptocercus rather than thehost genes.

The results of the present study, considered in lightof the above phylogenetic information, indicate thatthe older members of Cryptocercus are associated withhabitats dominated by evergreen forests. Cryptocercusclevelandi is distributed in forests dominated by ever-green trees such as Douglas fir, big cone Douglas fir,

and alpine fir, and is absent from deciduous standsnear the sites at which specimens were found. TheRussian C. relictus is distributed in evergreen forestsdominated by Korean fir and Korean pine, remnantsof the Arcto-Tertiary flora (Mamaev, 1973). However,C. relictus is capable, in experimental studies, of surviving and reproducing in deciduous host speciessuch as elm, cherry, oak, etc. (Mamaev, 1973). Thus,Mamaev (1973) wondered why C. relictus, whilecapable of surviving and reproducing in a variety ofhosts, has not spread to the mixed evergreen anddeciduous forests of eastern Russia. He attributed thelimited distribution of C. relictus and its restriction toKorean fir and Korean pine not to ‘narrow ecologicalvalence’ but to a limited dispersal capacity, an assump-



Figure 5. A phylogenetic tree for six of the seven Cryptocercus species depicting the inferred evolution of host and habitatassociation. The tree is based on parsimony analysis and DNA sequences of mitochondrial, nuclear and endosymbiontgenes (redrawn from Clark et al., 2001). Our analysis of habitat use showed that the basal species (C. relictus, C. cleve-landi) are associated with areas that are dominated by evergreen forests, while the Appalachian species (collectively theyoungest Cryptocercus species) are associated with areas dominated by deciduous and mixed forests. Similarly, C. darwini,the youngest among all species, occupies areas that are predominantly at low elevations (<397m ASL) while all otherspecies occupy areas that are predominantly at elevations of >398m ASL (see Fig. 2). Vegetational information for C. relic-tus is from Mamaev (1973); existing records (Bei-Bienko, 1935; Asahina, 1991) indicate that C. relictus occurs at relativelyhigher elevations.

tion for which there are no supporting data. Regard-less of the proximal factors, it is clear that C. relictus,like C. clevelandi, is associated primarily with ever-greens supporting our conclusion that the more basalCryptocercus species are associated with evergreenforests. It is worth noting that C. relictus and C. cleve-landi, which last shared a common ancestor 70–115million years ago (Clark et al., 2001), while still livingin predominantly evergreen forests, have adapted todifferent plant species, as outlined above.

In contrast, the Appalachian species have under-gone a transition in host association during the past50–90 million years. They are not limited to evergreenforests as C. clevelandi and C. relictus are; rather, theevolutionarily recent Appalachian Cryptocercus haveradiated into habitats that are dominated by deci-duous forests. This evolutionary trend is depicted inFigure 5.

There is also a discernable evolutionary trend in the elevational affinity of the various species. Crypto-cercus clevelandi, C. wrighti, C. punctulatus, and C.garciai occupy a habitat the majority of which liesbetween 398 and 1189m ASL. As mentioned above, theavailable data (Bei-Bienko, 1935; Asahina, 1991) indi-cate that C. relictus also occurs at relatively high ele-vations. However, the most apical species, C. darwini,occupies a habitat that is predominantly at lower ele-vations, i.e. <398m ASL. Thus, the evolutionary trendamong members of Cryptocercus has been a movementfrom a predominantly higher elevation habitat to onethat is largely at a relatively lower elevation, as shownin Figure 5.

In conclusion, we have demonstrated that Crypto-cercus species differ from one another in their habitatuse, host association, and population density. The differences reported here are consistent with theextensive genetic variation that has been reported previously among Cryptocercus species. In general, thebasal species (C. clevelandi, C. relictus) tend to occupyhabitats dominated by evergreen forests, while themore apical species (C. darwini, C. garciai, C. punc-tulatus, C. wrighti) tend to occupy habitats that are dominated by deciduous forests. Cryptocercusclevelandi resembles C. relictus in its habitat usedespite the fact that it is more closely related to theother Nearctic species than it is to C. relictus (Clarket al., 2001). Similarly, while all the other Nearcticspecies occupy a habitat that is predominantly at elevations of >398m ASL, the most recent species, C. darwini, occupies a low elevation (<398m ASL)habitat. Thus, we have identified differences in hostand habitat association among Cryptocercus speciesand also an evolutionary trend in those traits. Moredetailed observations on habitat use, host association,and distribution patterns of C. relictus and C. pri-marius must be made to fully comprehend the diver-

gence of Cryptocercus species in habitat use and hostassociation.

ACKNOWLEDGEMENTS

This study was supported by NSF grant DEB-9806710to S.K. Salary support for B.L.B. came from a NSF-LTER grant. We thank Konza Prairie BiologicalStation Remote Sensing Laboratory for use of equip-ment. This is journal article no. 01–350-J of theKansas State University Agricultural ExperimentStation.

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Evolution of host- and habitat association in the wood-feeding cockroach, Cryptocercus