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Orthoptera: Acrididae) Molecular Ecology (2005) 14, 2197–2205 doi: 10.1111/j.1365-294X.2005.02546.x HostBlackwell Publishing, Ltd. plant-associated genetic differentiation in the snakeweed grasshopper, Hesperotettix viridis (Orthoptera: Acrididae) G. A. SWORD,* A. JOERN† and L. B. SENIOR* *Northern Plains Agricultural Research Laboratory, United States Department of Agriculture, Agricultural Research Service, 1500 N. Central Ave., Sidney, MT, 59270, USA, †Division of Biology, Kansas State University, Manhattan, KS, 66506, USA Abstract Studies of herbivorous insects have played a major role in understanding how ecological divergence can facilitate genetic differentiation. In contrast to the majority of herbivorous insects, grasshoppers as a group are largely polyphagous. Due to this relative lack of inti- mate grasshopper–plant associations, grasshopper–plant systems have not played a large part in the study of host-associated genetic differentiation. The oligophagous grasshopper, Hesperotettix viridis (Thomas), is endemic to North America and feeds on composites (Asteraceae) within the tribe Astereae. Previous work has shown both preference and per- formance differences between H. viridis individuals feeding on either Solidago mollis or Gutierrezia sarothrae. Using 222 AFLP markers, we examined the genetic relationships among 38 H. viridis individuals feeding on these plants both in sympatry and allopatry. Neighbour-joining analysis resulted in two distinct host-associated clades with 71% boot- strap support for host-associated monophyly. Analyses of molecular variation (AMOVA) revealed significant genetic structuring with host plant accounting for 20% of the total genetic variance while locality accounted for 0%. Significant genetic differentiation was detected between S. mollis-feeders and G. sarothrae-feeders even when the two were present at the same locality. These results are consistent with observed differences in pref- erence and performance between H. viridis grasshoppers feeding on either G. sarothrae or S. mollis and indicate that H. viridis is comprised of at least two genetically distinct host plant-associated lineages. Keywords: AFLP, ecological divergence, Gutierrezia sarothrae, performance, preference, Solidago mollis Received 25 November 2004; revision accepted 17 February 2005 tion can be reduced if the resulting adaptations lead to pre- Introduction or postzygotic isolation mechanisms such as assortative The role of natural selection in promoting reproductive mating or inferior hybrid offspring (Bush 1994; Feder 1998; isolation is a cornerstone in models of speciation (Mayr Nagel & Schluter 1998; Nosil et al. 2002). This process, 1942, 1963) and has been the subject of renewed interest referred to as ecological speciation, initially forms genetically among evolutionary ecologists during the past decade (e.g. structured local demes and may eventually give rise to Schluter 1996a, b, 2001; Mopper & Strauss 1998; Orr & new species (Feder et al. 1998; Mopper & Strauss 1998; Via Smith 1998; Funk et al. 2002; Coyne & Orr 2004). Divergent 1999, 2001; Schluter 2001). selection pressures experienced by members of different Studies of herbivorous insects have played a central populations under alternate environmental conditions role in our understanding of the evolution of ecological can facilitate the evolution of reproductive isolation. Gene specialization (Jaenike 1990; Bernays & Chapman 1994; exchange between populations undergoing divergent selec- Thompson 1994; Mopper & Strauss 1998) and how such specialization may influence speciation (reviewed in Funk Correspondence: Gregory A. Sword, Fax: (406) 433 5038; E-mail: et al. 2002). A vast majority of herbivorous insects restrict [email protected] their diets to a closely related group of plant species and © 2005 Blackwell Publishing Ltd 2198 G. A. SWORD, A. JOERN and L . B . SENIOR are sometimes monophagous on single species (Bernays & be explained by either previous experience with the plant Chapman 1994; Bernays 1998). The intimate relationships from which they were collected or by environmental between specialist herbivores and their host plants in feed- parameters unrelated to host use (Traxler & Joern 1999). ing, oviposition, mate finding and predator avoidance The observed trade-offs in preference and performance make their populations particularly susceptible to disrup- on different hosts in H. viridis (Traxler & Joern 1999) indi- tive selection following shifts to novel host plants (Mopper cate the possibility of divergent selection for host plant & Strauss 1998; Berlocher & Feder 2002; Funk et al. 2002). specificity on the alternative hosts, S. mollis or G. sarothrae Host plant-associated ecological divergence among popu- (Futuyma & Moreno 1988; Via 1990; Joshi & Thompson lations that utilize different plants is often assessed in 1995). This negative correlation across host plants in pref- terms of traits such as preference to feed, mate, or oviposit erence and performance suggests that gene flow may in association with the different hosts as well a measures of be restricted between different host plant-associated performance in utilization of the different hosts such as forms. Using multilocus AFLP markers, we tested the null growth, survivorship and fecundity (Funk et al. 2002). hypothesis of no host plant-associated genetic structuring As a group, grasshoppers (Orthoptera: family Acrididae) of H. viridis grasshoppers using specimens retained from are somewhat unique among herbivorous insects in the original Traxler & Joern (1999) study along with indi- that they are largely polyphagous, feeding selectively on viduals from an additional allopatric, G. sarothrae-feeding host plant species from a number of unrelated plant population from New Mexico, USA. We observed signi- families (Otte & Joern 1977; Joern 1979; Chapman 1990; ficant host plant-associated genetic structuring of H. viridis Chapman & Sword 1997). Because of their polyphagy, most populations that is maintained even when the different grasshopper populations are not expected to experience host-associated forms co-occur at the same site. disruptive selection associated with host shifts. There are, however, some grasshopper species with restricted host Methods ranges and a small minority that are truly host specific (Otte & Joern 1977; Chapman 1990; Sword & Chapman Insect sampling 1994; Chapman & Sword 1997; Sword & Dopman 1999). Given that host plant specialization in grasshoppers Thirty second instar Hesperotettix viridis were collected off appears to be the exception rather than the rule, it is of multiple plants, one individual at a time, from populations interest to examine in grasshoppers the generality of the of each plant species dispersed within a radius of about mechanisms that in other herbivorous insects are thought 1000 m at two sites separated by 30 km in Nebraska, USA, to promote ecological diversification and reproductive (Keith and Arthur counties) as reported in Traxler & isolation. Joern (1999). The primary Keith County site has recently The snakeweed grasshopper, Hesperotettix viridis been destroyed by movement of earth because of new (Thomas) (Orthoptera: Acrididae: Melanoplinae), is native construction. For consistency across studies, we retain to North America. It is an oligophagous feeder that con- the terminology employed in Traxler & Joern (1999) to sumes only composites (Asteraceae) in the tribe Astereae describe the location and host plant affiliation of the insects (Mongkolkiti & Hosford 1971; Joern 1979, 1985; Parker & Root examined in this study. At the Keith County site, both 1981; Parker 1982, 1984). Traxler & Joern (1999) compared Solidago mollis and Gutierrezia sarothrae were utilized by populations of H. viridis from western Nebraska, USA, H. viridis. The 10 grasshoppers collected at this site from (Keith and Arthur counties) that fed primarily on one of S. mollis are referred to as K-S (#1–10) and the 10 grasshoppers two composites, either snakeweed, Gutierrezia sarothrae, collected from G. sartothrae are referred to as K-G (#1–10). or goldenrod, Solidago mollis. Using reciprocal transplant At the Arthur County site, only S. mollis was present and experiments, they found substantial divergence in both the insects from this site are referred to as A-S (#1–10). performance and preference traits between the different An additional 10 H. viridis specimens associated with host plant-associated grasshoppers. Individuals collected G. sarothrae were collected approximately 900 km from from G. sarothrae developed faster, survived longer and the Nebraska sites in Sevilleta, New Mexico, USA, and grew larger when fed G. sarothrae relative to those fed are referred to as S-G (#1–10). The same basic sampling S. mollis. Similarly, individuals collected from S. mollis devel- scheme described above was used in New Mexico, where oped faster and gained more weight on S. mollis than on grasshoppers were collected individually from multiple G. sarothrae. In this case, survivorship did not differ between plants. Insects were individually stored in ethanol. the two hosts. Paired choice experiments also revealed strong preferences for feeding on the host plant from AFLP protocol which they were collected. Importantly, these differences in performance and preference were found between indi- Hind femur muscle tissue from each of the 30 Nebraska viduals using different hosts at the same site and could not specimens was ground with sterile white quartz sand in a © 2005 Blackwell Publishing Ltd,
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