© 2001 by The Society for Integrative and Comparative Biology
Gall Flies, Inquilines, and Goldenrods: A Model for Host-race Formation and Sympatric Speciation1
1 Department of Biology, Bucknell University, Lewisburg, Pennsylvania 17837
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Host shifts and subsequent host-race formation likely play a more common role in the speciation of herbivorous insects than has generally been recognized. Our studies of the interactions of goldenrod host plants (Solidago: Compositae), the gall fly Eurosta solidaginis (Diptera: Tephritidae), and the stem- and gall-boring Mordellistena convicta (Coleoptera: Mordellidae) provide behavioral, ecological, and genetic evidence of insect host races that may represent incipient species formed via sympatric speciation. Eurosta solidaginis has developed genetically differentiated and reproductively isolated host races that are associated with the ancestral host Solidago altissima and the derived host S. gigantea. Conventional wisdom suggests that shifts even to closely related host plants are limited by host preferences or the inability to utilize a chemically and developmentally distinct host. However, our preliminary work with Eurosta from S. gigantea implies that host choice and gall induction do not deter a shift to S. canadensis. The galling of Solidago by Eurosta created a new resource that has led to a subsequent host range expansion by the stem-boring beetle. Mordellistena convicta from stems and galls are genetically distinct and likely shifted from stems to galls. Beetles from S. altissima versus S. gigantea galls exhibit assortative mating and higher preference for and/or performance on their natal host. The present-day distributions of the Eurosta host races and their behavioral isolating mechanisms do not suggest that geographic isolation was required for their formation; rather these characteristics suggest a sympatric mode of differentiation. Our findings lend credence to recent assertions that sympatric speciation may be an important source of biodiversity.
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INTRODUCTION |
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SYNOPSISINTRODUCTIONRESULTS AND DISCUSSIONCONCLUSIONReferences |
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Understanding the origin of biodiversity is of fundamental importance to evolutionary biology. Despite long study and debate, many details of the speciation process are not well understood, including whether geographic separation is necessary for speciation to occur. For phytophagous insects, many workers (Bush, 1994
; Larsson and Ekbom, 1995; Pellmyr and Leebens-Mack, 1998; Feder, 1998) have suggested that a host shift by a specialist herbivore to a closely related or chemically similar host-plant species is a significant, early step in the diversification process. Subsequent reproductive isolation due to host-associated mating may eventually lead to host-race formation and subsequently to speciation. This diversification scenario, however, has been controversial, and until recently limited data have been available to assess the roles of host shifts and host-race formation in the diversification of herbivorous insects.
Recent evidence suggests that host shifts and subsequent host-race formation by herbivorous insects are more common than has previously been recognized (Bush, 1969, 1994; Tauber and Tauber, 1989; Craig et al., 1993; Pratt, 1994; Crozier and Pamilo, 1996; Johnson et al., 1996; Romstock-Volkl, 1997; Sezer and Butlin, 1998; Wood et al., 1999). Host-race formation, as a first step towards sympatric speciation, promotes novel sub-populations that are reproductively isolated from their ancestral population via behavioral barriers (e.g., mate choice, host-plant choice) rather than by geographic barriers (Feder et al., 1989; Craig et al., 1993, 1997; Crozier and Pamilo, 1996; Kawecki, 1998; Berlocher, 1999). Behavioral barriers can be created when sub-populations of herbivores have strong and specific host-plant preferences and/or positive assortative mating. In some examples (e.g., Craig et al., 1993, 1997, 2001; Itami et al., 1997), strong host-plant association is tightly coupled with effective assortative mating to produce virtually complete reproductive isolation under sympatric conditions. Such coupling of host-plant choice and mate choice is common among herbivorous insects because mating frequently occurs on the host plants. Although not required, such coupling markedly increases the likelihood of host-race formation.
Many of the details of host-race formation have been elegantly documented for the tephritid fly Rhagoletis pomonella since Guy Bush first argued the importance of host-race formation in generating biodiversity (e.g., Bush, 1969; McPheron et al., 1988; McPheron and Han, 1997; Feder, 1998; Berlocher, 1998, 1999). Over the past decade, host races have been documented in another tephritid fly, the goldenrod ball gall inducer Eurosta solidaginis (Waring et al., 1990; Craig et al., 1993, 1997, 1999, 2000, 2001; Brown et al., 1995, 1996). As a gall inducer, this herbivore has an intimate association with its host plant which, when taken with the insect's mating and oviposition behavior, creates a strong coupling of host-plant choice and mate choice (Craig et al., 1993; Abrahamson et al., 1994; Abrahamson and Weis, 1997). As a consequence, a host shift from the ancestral host-plant Solidago altissima to the novel host-plant S. gigantea has resulted in the reproductive isolation and differentiation of two host races (Abrahamson et al., 1994; Craig et al., 1994, 2001).
Such host shifts to closely related plants often appear to be limited by herbivore host-plant preference or an herbivore's inability to utilize a chemically and developmentally distinct host. However, for Eurosta that induce galls on the closely related but infrequently attacked S. canadensis, our on-going studies imply that host choice and gall induction do not restrain a range expansion to S. canadensis (unpublished data, A.V.W.). Understanding the factors that both promote and restrain host shifts and host-race formation is fundamental to our comprehension of the speciation of herbivorous insects.
Studies of Rhagoletis and Eurosta, as well as findings with other insects (e.g., Menken, 1981; Abe, 1991; Singer et al., 1993; Guldemond et al., 1994; Sezer and Butlin, 1998; Wood et al., 1999), make clear that host-race formation occurs frequently and that it is an important evolutionary mechanism that creates biodiversity. In this paper, we report on how the formation of galls by the goldenrod gall fly has promoted a host shift and differentiation of the beetle Mordellistena convicta. Below, we provide a summary of the ecological, behavioral, and genetic attributes of host-race formation by the gall-inducer E. solidaginis, furnish an overview of the pattern of genetic differentiation and reproductive isolation within the beetle, and discuss the implications for sympatric speciation.
Host-race formation criteria
A host race has been defined as "a population of a species that is partially reproductively isolated from other conspecific populations as a direct consequence of adaptation to a specific host" (Diehl and Bush, 1984). Jaenike (1981) more narrowly defined host races as being "restricted solely or primarily because of different host preference." Using these definitions, we have proposed criteria or lines of evidence that may exist in order for conspecific, herbivorous insects that consume different host plants to be considered host races (Abrahamson and Weis, 1997):
- Sympatry—Populations must be sympatric (Jaenike, 1981).
- Genetic Differences—If host-race formation has occurred, then gene flow among host-associated populations should be low and genetic differentiation between sympatric, host-associated populations is likely (Feder et al., 1988; McPheron et al., 1988; Waring et al., 1990). Furthermore, host-race formation should eventually produce diagnostic patterns of phylogenetic relationships distinguished by all populations of the widespread "ancestral" race forming a paraphyletic group, whereas populations of the "derived" race arise from within the ancestral race clade (Brown et al., 1996).
- Assortative Mating due to Host-Plant Preferences—Host-associated mating would promote host-associated reproductive isolation. The coupling of mating and habitat or host choice can remove the selection-recombination antagonism envisioned by some models of sympatric speciation because the same genes are selected for in both host selection and assortative mating (Diehl and Bush, 1989; Abrahamson and Weis, 1997).
- Oviposition Preference for Plant—Oviposition preferences for different host plants by host races, whether genetically or environmentally determined, are essential for a host shift and host-race formation (Bush, 1975; Futuyma, 1983; Diehl and Bush, 1989). Many herbivorous insects are preadapted to use closely related plant species; hence an environmentally or genetically determined change in preference could lead to an immediate and viable host shift (Bush, 1975).
- Allochronic Isolation—Differential emergence times of galling and boring insects from alternative host plants (allochronic emergence) can promote reproductive isolation and host-race formation (Bush, 1969; Tauber and Tauber, 1989; Wood and Keese, 1990; Craig et al., 1993). Because many adult insects are relatively short lived, host-associated emergence differences of only a few days can dramatically affect the availability of mates from the same or alternative host plants.
; Tauber and Tauber, 1989; Abrahamson et al., 1994; Craig et al., 1994, 2000, 2001; Brown et al., 1995; Hess et al., 1996; Itami et al., 1997). For example, competition and parasitism are higher on ancestral versus novel host plants in the Rhagoletis pomonella-hawthorn-apple host-race complex (Averill and Prokopy, 1987; Feder, 1995; Feder et al., 1995). Thus, Rhagoletis that feed on apple (the derived host plant) experience reduced competition and parasitism as a result of a host shift. |
RESULTS AND DISCUSSION |
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Evidence for Eurosta host races
Eurosta solidaginis (Diptera: Tephritidae) is a univoltine, gall-inducing herbivore that is native to North America. Adult flies typically emerge from galls, mate, and females oviposit into the apical buds of host plants in May. Adults do not feed and typically live as little as a few days to perhaps as many as 10 days. Galls begin to appear 3 wk after oviposition and galls are fully grown by mid-July. The larva reaches peak mass by September and overwinters within its gall as a third-instar larva. Galls of E. solidaginis commonly occur on the stems of Solidago altissima (Compositae) throughout the host-plant's range from the southeastern USA north into Canada and west across the plains. While Eurosta does not attack the closely related S. gigantea throughout most of its range (which is very similar to that of S. altissima), gall flies frequently infest S. gigantea across the northern tier of the USA and southern Canada (Waring et al., 1990
; Abrahamson and Weis, 1997).
Where galls occur on both S. altissima and S. gigantea, galled ramets of these two host plants are often found interdigitated; thus making the host-associated gall fly populations truly sympatric (Craig et al., 1993). We will refer to these host-associated gall fly populations as "altissima" flies and "gigantea" flies.
Results of allozyme and mtDNA studies provide unequivocal evidence of genetic differentiation of the "altissima" and "gigantea" fly populations (Waring et al., 1990; Brown et al., 1996). The greater heterozygosity of loci in "altissima" populations and the patterns of clade formation based on mtDNA sequences of cytochrome oxidase I & II suggest that the host shift occurred from S. altissima to S. gigantea and that the shift took place in the northeastern USA (Waring et al., 1990; Brown et al., 1996).
Gene flow between the two host races is reduced by a number of mechanisms including emergence time, assortative mating, adult oviposition choice, and reduced hybrid performance (Craig et al., 1993, 1997, 2000, 2001). For example, emergence times of the two host races are allochronic with the emergence of "gigantea" flies occurring on average 10–13 days earlier than "altissima" flies (Craig et al., 1993; Abrahamson et al., 1994). Furthermore, "altissima" and "gigantea" flies demonstrate strong assortative mating in the presence of host plants (Craig et al., 1993). Gall flies associate with their natal hosts and mate on these plants, consequently the host plants mediate the meeting of mates. Disruptive selection against hybrids may further reduce gene flow between "altissima" and "gigantea" flies. Although the host races form hybrids when forced in captivity, the hybrids and their backcross progeny perform more poorly than parental types on all host plants (Craig et al., 1997, 2000, 2001; Itami et al., 1997).
The survivorship of the derived host race attacking S. gigantea may be increased by reduced natural enemy attack and diminished competition. Parasitism may be higher in the ancestral "altissima" host race than in the "gigantea" host race. A survey of goldenrod fields that included sympatric "altissima" and "gigantea" populations in Vermont and New Hampshire found, on average, that Eurosta survivorship was higher on the derived host plant, S. gigantea, than on the ancestral host plant, S. altissima. This improved survivorship was a consequence of reduced natural enemy attack from the parasitoid wasp Eurytoma obtusiventris and from downy woodpeckers (Abrahamson et al., 1994; Brown et al., 1995). Eurytoma obtusiventris appears to use host-plant cues to locate its prey so a shift to a novel host plant may provide reduced enemy space (Brown et al., 1995). Furthermore, larval competition among flies attacking the ancestral host S. altissima appears to be more intense than among flies infesting S. gigantea because of higher levels of oviposition on S. altissima buds (Abrahamson et al., 1994; Hess et al., 1996; Craig et al., 2000).
Barriers to host shifts
The shift of Eurosta from S. altissima to S. gigantea raises the question of what prevents host shifts—that is, why did this shift occur only once and why aren't such host shifts even more common? There have been occasional reports of E. solidaginis galls on S. canadensis. Our extensive experience with E. solidaginis galls in New England (where both S. altissima and S. gigantea host Eurosta) suggests that Eurosta galls occur very infrequently on S. canadensis. However, we have occasionally encountered fields (e.g., Missisquoi National Wildlife Refuge, Swanton, Vt.) with pockets of galls on S. canadensis (personal observations, A.V.W., W.G.A.). Oviposition-choice tests show that the derived "gigantea" host race, but not the "altissima" host race, will oviposit on S. canadensis at fairly high rates even when the respective natal hosts are available (unpublished data, A.V.W.). This finding corresponds to the observation that "gigantea" flies are in general considerably more promiscuous in both mating and oviposition (Craig et al., 2001; personal observations, W.G.A., M.D.E., A.V.W.). An experiment to determine whether "gigantea" flies could form galls on S. canadensis found that galls were induced at a higher rate on S. canadensis than on S. gigantea (unpublished data, A.V.W.). This latter finding suggests that "gigantea" flies may be preadapted to use S. canadensis. However, S. canadensis has an appreciably earlier growth phenology than either S. gigantea or S. altissima (Abrahamson and Weis, 1997). Because gall induction requires the availability of actively growing undifferentiated plant tissue (Abrahamson and Weis, 1987), this early phenology may lessen the probability of attack by gall flies and cause the "window of vulnerability" to gall formation to close sooner. If so, gall flies attacking S. canadensis may be under selection for earlier emergence. These "canadensis" gall flies may provide an opportunity to study the early stages of a host shift.
Differentiation of Mordellistena convicta
A native North American species of Mordellistena, a large genus of stem-boring beetles, has long been known as an inhabitant of the goldenrod ball galls induced by the larva of E. solidaginis on S. altissima. This beetle has been variously identified as M. unicolor LeConte (e.g., Ping, 1915; Uhler, 1951), M. nigricans Melsh. (e.g., Harrington, 1895), M. aspersa Melsh. (Liljeblad, 1945), Mordellistena sp. (e.g., Milne, 1940), and lately as M. convicta (Ford and Jackman, 1996). Adult females lay their eggs on the surfaces of newly formed galls and the larvae bore into galls where they develop by feeding on the parenchymal tissues induced by the gall fly larva (Ping, 1915). Although these beetles can complete their development on this diet of plant tissue, the beetles typically chew into the central chambers of the galls where they consume the fly larvae (Uhler, 1951; Abrahamson and Weis, 1997). In one 14-yr study, beetles consumed the fly larvae in an average of 73.2% of the galls in which beetles were found (Uhler, 1961).
Mordellistena convicta has also been reared repeatedly from Eurosta galls on S. gigantea (Harrington, 1895; Abrahamson et al., 1989; Sumerford and Abrahamson, 1995). Furthermore, Cappuccino (1992) reported M. convicta from the stems of S. altissima. Consequently, we cultured extensive numbers of stems from various goldenrod species and have reared M. convicta from the stems of S. altissima, S. gigantea, Euthamia graminifolia (identification of beetles by J. Jackman), S. rugosa, and S. juncea (unpublished data, C.P.B.). Ford and Jackman (1996) also report its presence in Aster vimineus, Ambrosia artemisiifolia, and Xanthium strumarium. These findings suggest that either M. convicta is polyphagous and attacks a variety of plant organs and host-plant species or exists as differentiated sub-populations according to host organ and/or host-plant species.
These observations suggested the hypothesis that reproductively isolated populations of M. convicta exist in the stems and galls of S. altissima or S. gigantea. We tested this hypothesis using the same criteria for determining the existence of host races as we employed for Eurosta host races. Specifically, we examined whether the host-plant and host-organ associated beetle populations exist in sympatry, whether there is evidence of genetic differentiation among host-plant and plant-organ associated populations, whether host-plant and plant-organ associated populations have different emergence times, whether females prefer to oviposit on natal host plants and plant organs, whether offspring perform better on natal host plants and plant organs, and whether assortative mating occurs according to natal host plant and plant organ. Our behavioral studies of these M. convicta sub-populations show that the beetles' mating and oviposition behaviors may act to reduce gene flow among sub-populations and could facilitate diversification (unpublished data, M.D.E., C.P.B.).
As described above, "altissima" and "gigantea" galls occur sympatrically across the northern tier of the USA and southern Canada (Abrahamson and Weis, 1997). Eurosta galls containing M. convicta larvae frequently occur on interdigitated ramets of S. altissima and S. gigantea in our New England study sites. Furthermore, M. convicta larvae occur sympatrically within the same plant ramet—occurring within the stem and that stem's gall on both host plants (personal observations, C.P.B., W.G.A., M.D.E.). Clearly these sub-populations meet the criterion for sympatry.
A survey of allozymes found five variable and consistently scorable enzymes: AAT (EC 2.6.1.1
[EC]
), AK (EC 2.7.4.3
[EC]
), IDH (EC 1.1.1.42
[EC]
), MDH (EC 1.1.1.37
[EC]
), and PGM (EC 5.4.2.2
[EC]
) among the stem- and gall-boring beetle populations (unpublished data, C.P.B.). At the MDH locus, there were significant allele frequency differences between stem and gall populations (Table 1), but none of the five loci studied distinguished between the sub-populations in the stems of the two Solidago species or between the sub-populations in the two galls. The genetic difference between stem and gall beetles suggests that M. convicta has shifted at least once, and given that M. convicta is a stem-boring species, and that stem-boring is common in Mordellistena (Ford and Jackman, 1996) gall-boring seems to be the derived trait and thus the shift occurred from stem to gall.
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2 (stem vs. gall) = 505.9 (df = 1), P < 0.0001, (n) = sample sizeThere is a possibility for reduced gene flow between the stem and gall beetle sub-populations because M. convicta emerging from S. altissima stems in Pennsylvania appeared an average of 2 wk earlier than did beetles emerging from S. altissima galls (unpublished data, C.P.B.). Furthermore, the phenology of gall beetle populations also differed: beetles from New England emerged from S. gigantea galls on average 1.1 days earlier than from S. altissima galls. However, these results should be viewed cautiously even though they were statistically significant. Such allochronic emergence may not be biologically important because adult M. convicta can survive for three months (Weis and Abrahamson, 1985
; Jackman and Nelson, 1995). Mordellistena adults frequent the flowers of numerous plants to feed on pollen. Long adult life and the possibility that males and females of different sub-populations meet while feeding create the prospect for gene flow among sub-populations. Likely more important to the reproductive isolation of beetle sub-populations was our finding that M. convicta from galls assortatively mate according to their natal host plant (Fig. 1; unpublished data, M.D.E.). We conducted a mate-choice experiment by providing focal beetles with a choice of two potential mates: one beetle from their natal host plant and one reared from galls on the alternate host plant. Each beetle was marked with a tiny dot of model paint (Testors®) applied with a bristle from a fine paintbrush (colors: white, red, and yellow, randomized for each trial). We placed marked beetles into a 15-cm diameter petri dish under standard florescent lighting at room temperature. We monitored the behavior of all beetles for 2 hr and recorded the host-plant origin of beetles that copulated with the focal animal. We conducted 38 trials with focal beetles reared from S. altissima galls and 62 trials with focal beetles reared from S. gigantea. When offered a choice of mates from the galls of their natal host plant or the alternate host plant, "altissima" beetles were much more likely to mate with another "altissima" beetle than with a "gigantea" beetle and vice versa.
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Furthermore, adult beetles differentially oviposit and/or their offspring survive better in their natal host-plant species. For example, in both no-choice and choice tests, we found that offspring emerged more frequently from galls of their parents' natal host plant than from galls of the alternate host plant. In no-choice tests, beetles reared from S. gigantea galls or S. altissima galls were caged with galled ramets of either S. gigantea or S. altissima. Beetles reared from S. gigantea galls produced offspring that emerged only from galls on S. gigantea and beetles reared from S. altissima galls produced offspring that emerged only from S. altissima galls. Likewise, when beetles were given a choice and caged with both S. gigantea and S. altissima galled ramets, S. gigantea beetles produced offspring that emerged at higher rates from S. gigantea galls and S. altissima beetles produced offspring that emerged at higher rates from S. altissima galls (unpublished data, M.D.E.).
Finally, there is evidence that the host shift from stems to galls may be maintained by enemy-reduced attack on the derived gall-dwelling beetle populations. We identified a high level of mortality to stem beetles due to the attack of the chalcid parasitoid Tetrastichus ainsliei Gahan (Eulophidae). However, this parasitoid was completely absent from all sampled gall beetle populations (unpublished data, C.P.B.).
Implications for sympatric speciation
We argue that host shifts and subsequent host-race formation such as described here are important, early steps leading to diversification and speciation in herbivorous insects. However, host-race formation via host shifts has been well documented in a limited number of examples. The addition of yet another example from Mordellistena suggests that the biodiversity of herbivorous insects may in part be due to sympatric processes.
Our ecological, behavioral, and genetic studies of the Eurosta gall inducer and Mordellistena stem- and gall-boring beetle illustrate the existence of host and organ races, and offer insights into the conditions necessary for their formation. Colonization of Eurosta's galls by Mordellistena stem beetles has facilitated the differentiation of stem- and gall beetle sub-populations. It is conceivable that the gall fly's host shift from S. altissima to S. gigantea created a new resource for the beetle that will provide the opportunity for the differentiation of beetle sub-populations within the galls of different Solidago species. Further research is needed to establish how closely linked the beetle differentiation is to the fly shift, specifically whether there was a gall-to-gall shift rather than simultaneous colonization and if so, the direction of the shift. Our results lend further credence to recent assertions that sympatric speciation via host-race formation may be an important source of biodiversity (Bush, 1994; Berlocher, 1998, 1999).
Our behavioral work with Eurosta implies that the coupling of mate choice and host-plant choice may make it easier for host races to form via their combined effect on the reduction of gene flow among host-associated populations. For this gall inducer, genetic differentiation likely is maintained by disruptive selection for host-plant use because the F1 and F2 hybrids, as well as backcross progeny, exhibit reduced performance relative to the pure host-race offspring (Craig et al., 1997, 2001). The results from our Mordellistena studies imply that diversification can occur if assortative mating and oviposition preference and/or offspring survival promote reproductive isolation. Finally, for both Eurosta and Mordellistena, the reduction of mortality to the derived host-associated populations due to partial escape from a natural enemy may maintain, if not promote, the derived population. The critical consequence for both Eurosta and Mordellistena is that behavior, rather than geography, limits gene flow and hence may enable the genetic differentiation of sub-populations. The behavioral, ecological, and genetic attributes of these sub-populations are currently such that geographic isolation may not be a prerequisite to their formation (Abrahamson and Weis, 1997). Consequently, there is no need to invoke allopatric conditions to explain the patterns of variation seen in both the gall inducer and its inquiline beetle. The results detailed above suggest a sympatric mode of differentiation suggesting that these sub-populations have originated in sympatry.
The concept of sympatric speciation by host-race formation remains contentious because of the restrictive conditions that many workers have suggested are required, based on models using assumptions that may not be true (Tauber and Tauber, 1989). These restrictions make it improbable that sympatric speciation could ever occur (Futuyma, 1983; Futuyma and Peterson, 1985; but see Johnson et al., 1996; Kawecki, 1998 for arguments that loosen these restrictions). However, findings with Rhagoletis (e.g., Feder and Filchak, 1999), as well as those summarized above for Eurosta and Mordellistena suggest that some of these restrictions can be relaxed. We can never be certain that present-day ecological and genetic conditions match past circumstances or that present population-level situations can be extended to explain larger-scale, phylogenetic patterns (Rausher, 1988). Furthermore, because speciation is a historical process, studies like ours can only suggest the most parsimonious explanation of how speciation has proceeded (Wood and Keese, 1990). Hence, we will never know all the details of the genetic differentiation of sub-populations of Eurosta and Mordellistena. Nonetheless, studies like those reported here provide important insights into the process of herbivorous insect speciation.
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CONCLUSION |
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Conventional wisdom is that new species arise when geographic barriers divide an existing species into two or more isolated populations. When mountains, oceans, or other barriers prevent the exchange of genes between the isolated populations, each evolves along an independent path. If geographic isolation lasts long enough, the populations may diverge to a point that interbreeding is no longer possible—one species divides into several. With an herbivore such as Eurosta, barriers to gene exchange arise not out of geography, but out of behavior. When mating occurs only on the host, a sub-population consistently choosing one host will not mate with that choosing the other. For Mordellistena, assortative mating according to natal host plant coupled with preferential oviposition by females and/or differential offspring survival on their natal host plant appear to contribute to its formation of sub-populations (unpublished data, M.D.E.). Our results support the suggestion that differentiation and subsequent speciation may occur in the absence of geographic separation (Johnson et al., 1996
). Many have argued that the conditions for sympatric speciation are too restrictive for it to be important. Our work on Eurosta and Mordellistena indicates that mating and oviposition behaviors can provide a barrier to gene exchange. Given that over 25% of all species are herbivorous insects (Strong et al., 1984), sympatric speciation may be an important source of the earth's biodiversity.
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ACKNOWLEDGMENTS |
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The symposium, "An Integrative Approach to the Studies of Terrestrial Plant-Animal Interactions," was supported by the Society for Integrative and Comparative Biology; we are grateful for this support. The author's research was supported by NSF grants DEB-9710109 to W.G.A. & J.T. Cronin, DEB-9806339 to W.G.A. and M.D.E., and DEB-9981330 to W.G.A. and A.V.W. We heartily thank our colleagues Jonathan Brown, Tim Craig, Jim Cronin, John Horner, Joanne Itami, Shellee Morehead, and Gwen Waring for their appreciable contributions to many of the findings reported here. C. Abrahamson, M. Bremer, K. Caufman, J. Cronin, K. Hyland, J. Jackman, A. Kienle, I. Kralick, S. Marshall, A. Mehalow, G. Melika, H. Petre, S. Sidlow, L. Tyrell, L. Young, and an anonymous reviewer provided technical and field support, and/or helpful comments.
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FOOTNOTES |
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1 From the Symposium An Integrative Approach to the Study of Terrestrial Plant-Animal Interactions presented at the Annual Meeting of the Society for Comparative and Integrative Biology, 5–8 January 2000, at Atlanta, Georgia.
2 E-mail: abrahmsn{at}bucknell.edu
3 Present address of M. D. Eubanks is Department of Entomology and Plant Pathology, Auburn University, AL 36849
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References |
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