Journal of Heredity Advance Access originally published online on June 30, 2005
Journal of Heredity 2005 96(5):572-575; doi:10.1093/jhered/esi075
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Brief Communication |
Population Genetics of Wood-Feeding Cockroaches in the Genus Cryptocercus
From the Department of Entomology, Kansas State University, Manhattan, KS 66506 (Aldrich and Kambhampati) and the Department of Entomology, Iowa State University, Ames, IA 50011 (Krafsur)
Address correspondence to Srini Kambhampati at the address above, or e-mail: srini{at}ksu.edu.
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Abstract |
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Members of the genus Cryptocercus are xylophagous, wingless, subsocial cockroaches that inhabit decaying logs in temperate forests. Given their winglessness, subsocial living, and the patchy distribution of food resources (decomposing logs), it is likely that Cryptocercus populations are substructured. Allozyme variation at eight polymorphic loci was assayed for 10 subpopulations of Cryptocercus darwini and 13 subpopulations of Cryptocercus wrighti, both of which are distributed in the Appalachian Mountains. The mean FIS was 0.13 and FST was about 0.25 for both C. darwini and C. wrighti. The relatedness among individuals of a subpopulation of both species was not significantly different from that expected among full sibs. In terms of how genetic variation is partitioned, C. darwini and C. wrighti differed from each other substantially. Most of the genetic variation occurred among subpopulations of C. wrighti in the same region and among subpopulations of C. darwini in different regions. We discuss the factors that may have contributed to the observed similarities and differences in the breeding structure of the two species.
Members of the genus Cryptocercus (Dictyoptera: Cryptocercidae) are subsocial, xylophagous cockroaches that inhabit damp, decaying logs of temperate forests in the Palearctic and Nearctic. Cryptocercus are organized into subsocial groups in which one or both parents care for nymphs in various stages of development (Cleveland et al. 1934; Nalepa 1984). Unlike eusocial insects, there is no division of labor in Cryptocercus colonies. Adult male and female Cryptocercus are wingless, suggesting limited dispersal. Thus it is likely that social organization, behavior, specialized diet, and winglessness of Cryptocercus may lead to substructured populations and high relatedness among individuals within a subpopulation.
Our objective was to quantify and compare the breeding structure of Cryptocercus darwini and Cryptocercus wrighti, two species that share similar life histories but diverged from each other more than 20 million years ago (Clark et al. 2001). These two species inhabit regions composed of deciduous or mixed forests in the Appalachian Mountains; about 55% of the area inhabited by C. darwini is less than 400 m above sea level (ASL), while 80% of the habitat occupied by C. wrighti is more than 400 m ASL (Kambhampati et al. 2002). In addition, the distribution of C. darwini includes wet and warm climates relative to that of C. wrighti (Kambhampati S and Peterson AT, unpublished data). Whereas C. darwini has a widespread distribution, C. wrighti has a relatively limited distribution (Aldrich et al. 2004; Steinmiller et al. 2001). Since no studies have been performed to quantify the dispersal of Cryptocercus, it is not known whether interspecific differences in breeding structure exist because of a propensity to disperse, distribution of resources, historical factors, genetic and ecological differences, or divergence of several million years. In this study we examine if the above factors are reflected in differences in breeding structure of the two species.
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Materials and Methods |
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Insect Collection and Allozyme Analysis
Cryptocercus were sampled from 50 sites in the Appalachian Mountains during July 2001. Twenty-three collection sites (10 of C. darwini, 13 of C. wrighti) contained an adequate number of individuals for this study (Figure 1). At each collection site, Cryptocercus were sampled from a single log until all individuals were collected. If sufficient individuals were not found in a single log, adjacent logs were sampled to obtain the desired sample size (
40 individuals per site). Samples from 10 of the 23 sites (5 each of C. darwini and C. wrighti) contained sufficient individuals collected from a single log (constituting one or more families) and those from the remaining sites consisted of individuals collected and pooled from two or more logs. Thus, in this article, a subpopulation comprises the individuals collected at a given sampling site consisting of members of a single or multiple colonies. At each collection site, adults were placed in 100% ethanol for species identification using DNA analysis [methods and results reported by Aldrich et al. (2004)]; nymphs were preserved in liquid nitrogen for allozyme analysis. Eight polymorphic (95% criterion; Hartl and Clark 1997) allozyme loci identified for Cryptocercus by Aldrich et al. (2004) were utilized to quantify genetic variation within and among subpopulations of the two species. Nymphs were used in this analysis because of their relative abundance compared to adult individuals and to discount any variation in allele frequencies among members of different age classes.
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Data Analyses
The expected and effective number of alleles (Kimura and Crow 1964) at each locus, percent polymorphic loci, observed heterozygosity, and expected heterozygosity for all loci (Nei 1973) were estimated using POPGENE version 1.3 (Yeh et al. 1998). F-statistics were calculated using FSTAT version 2.9.3 (Goudet 2001). Genetic variation in each species was partitioned into four hierarchical levels: within (FIR) and among (FRT) regions, and within (FIS) and among (FST) subpopulations. Analyses were also performed on each region individually at two hierarchical levels: within (FIS) and among subpopulations (FSR) within a region. C. darwini subpopulations were partitioned into three regions and C. wrighti subpopulations were partitioned into two regions based on spatial distribution of the subpopulations and pairwise FST estimates (Figure 1). Student's t-tests were used to assess if FIS estimates differed significantly from zero. RELATEDNESS version 5.0.8 (Queller and Goodnight 1989) was used to estimate the mean relatedness of individuals within subpopulations relative to regions, subpopulations relative to the total population, and regions relative to the total population. Student's t-test was used to assess if mean jackknifed relatedness estimates differed significantly from 0 and 0.5 (unrelated individuals and full siblings, respectively; Goodisman and Crozier 2001).
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Results and Discussion |
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Of eight loci examined, two loci (DIA and IDH) were polymorphic in only one of the two species (Table 1). The number of individuals assayed per subpopulation ranged from 16 to 42 per locus with a mean of 33 ± 2.1 (S.E.). The observed heterozygosity varied considerably among loci, ranging from essentially 0 for some loci to 0.6 for EST in both C. darwini and C. wrighti (Table 1). In most cases the observed heterozygosity was smaller than that expected under Hardy-Weinberg equilibrium. Deviations from Hardy-Weinberg equilibrium are likely the result of pooling separate breeding units (families) during our analysis, leading to the Wahlund effect (Hartl and Clark 1997). All 10 subpopulations (5 of C. darwini, 5 of C. wrighti) that were collected from single logs had heterozygosity values that deviated from Hardy-Weinberg expectations and 9 of those 10 (4 of C. darwini, 5 of C. wrighti) displayed FIS values significantly greater than zero. This suggests that all individuals within a log are not part of a single breeding population.
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The mean departure from random mating among regions (FRT) and the mean departure from random mating among subpopulations within regions (FSR) differed between the two species, whereas the mean departure from random mating among subpopulations (FST) and the mean departure from random mating within subpopulations (FIS) were similar between them (Table 2). Estimates of FST, FSR, and FRT for C. darwini and C. wrighti were significantly different from zero. Overall the FIS estimates for both species (combined over all subpopulations; Table 2) were not significantly different from zero (C. darwini: t9 = 0.39, P = 0.71; C. wrighti: t12 = 1.13, P = 0.30). All 23 subpopulations had positive FIS values; of these, 18 (78%; 7 of 10 C. darwini subpopulations and 11 of 13 C. wrighti subpopulations) were significantly greater than zero (P < 0.05). Gene flow estimates (Nm = 0.25(1 – FST)/FST) averaged over all loci suggested that approximately one reproductive cockroach migrates into a subpopulation every 1.5 generations for both species.
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Of the total genetic variability for C. darwini, 59% of the total genetic variation was distributed among regions and 9% among subpopulations within a region. In contrast, only 16% of the genetic variation is to be found among regions and 60% among subpopulations within a region for C. wrighti. We do not believe this is an artifact of the average distance among the sampled subpopulations and the distance between regions which were similar for both species (mean distance among subpopulations of C. darwini and C. wrighti: 22 km and 29 km, respectively; mean distance between regions for C. darwini and C. wrighti: 143 km and 123 km, respectively). Thus it is possible that the interspecific differences in partitioning of genetic variance reflect either previously undetected interspecific differences in propensity to disperse or result from historical and biogeographical patterns.
The average relatedness among individuals within a subpopulation was similar (0.37), and significantly greater than 0 (C. darwini: t9 = 2.30, P < 0.01; C. wrighti: t12 = 3.14, P < 0.001), but not significantly different from the 0.5 expected for full sibs for both species (C. darwini: t9 = 0.64, P = 0.26; C. wrighti: t12 = 1.03, P = 0.15). However, the subpopulations of the two species differed from one another in the mean relatedness among individuals within regions relative to the total population (C. darwini: r = 0.34 ± 0.17; C. wrighti: r = 0.08 ± 0.03). Since a majority of the subpopulations in this study consisted of more than one family, these results suggest that the movement of Cryptocercus within a sampling site is limited. If there is considerable movement of individuals among widely dispersed logs, the average relatedness among individuals within a log, or a set of logs in the vicinity of one another, would be between 0 and 0.5 (expectation in an outbred population). However, our estimates of mean relatedness among individuals even from different families and logs approximated 0.5.
Our results suggest that much change has occurred in the breeding structure of C. darwini and C. wrighti since their divergence about 20 million years ago (Clark et al. 2001). Two factors that may have contributed to the observed differences in breeding structure are ecological niches and historical factors. Both Kambhampati et al. (2002) and Kambhampati and Peterson (unpublished data) conclude that ecological niches of C. darwini and C. wrighti differ from each other. These factors may have an impact on the availability of logs suitable for colonization, thereby influencing the observed genetic variance patterns. Historical patterns of population expansion and contraction could also result in the patterns of genetic variation observed here. C. darwini and C. wrighti differ substantially in the extent of their distributions (Aldrich et al. 2004; Steinmiller et al. 2001). If these differences in distribution are the result of a recent, rapid expansion by C. darwini, one might expect considerable differences in their population structure.
The subsocial behavior of Cryptocercus is also a potential factor limiting the dispersal capacity of these insects. Cryptocercus rely on intestinal, cellulase-producing protozoans for the digestion of cellulose (Cleveland et al. 1934). However, newly hatched nymphs lack these protozoans and nymphs (until the third or fourth instar) lose their symbionts along with the hindgut lining at each ecdysis. Nymphs must therefore acquire and reacquire the gut protozoa from their parents through proctodeal feeding before they can digest wood. The process of reinfestation requires an extended period of parental care, lasting 3 or more years (Nalepa 1984) and prevents parents from departing their colony until the young are capable of independently digesting wood. Therefore social interactions within Cryptocercus ensure the survival of the offspring, yet the same behavior restricts the movement of these insects.
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Acknowledgments |
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We thank the U.S. Forest Service, the National Park Service, and the states of Alabama, Georgia, North Carolina, Kentucky, South Carolina, Tennessee, Virginia, and West Virginia for issuing permits to collect cockroaches. This study was funded by a National Science Foundation grant (DEB-9806710 to S.K.). This is journal article number 04-266-J of the Kansas Agricultural Experiment Station.
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Footnotes |
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Corresponding Editor: Rob DeSalle
Received January 1, 2005
Accepted March 3, 2005
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References |
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