Spatial Structure and Habitat Variation in a Grasshopper Hybrid Zone
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Evolution, 55(9), 2001, pp. 1832±1843 SPATIAL STRUCTURE AND HABITAT VARIATION IN A GRASSHOPPER HYBRID ZONE JON R. BRIDLE,1,2 STUART J. E. BAIRD,3,4 AND ROGER K. BUTLIN1,5 1Centre for Biodiversity and Conservation, School of Biology, University of Leeds, LS2 9JT, United Kingdom 3University of Queensland, Brisbane, Queensland 4072, Australia 4E-mail: [email protected] 5E-mail: [email protected] Abstract. A hybrid zone between the grasshoppers Chorthippus brunneus and C. jacobsi (Orthoptera: Acrididae) in northern Spain has been analyzed for variation in morphology and ecology. These species are readily distinguished by the number of stridulatory pegs on the hind femur. Both sexes are fully winged and inhabit disturbed habitats throughout the study area. We develop a maximum-likelihood approach to ®tting a two-dimensional cline to geo- graphical variation in quantitative traits and for estimating associations of population mean with local habitat. This method reveals a cline in peg number approximately 30 km south of the Picos de Europa Mountains that shows substantial deviations in population mean compared with the expectations of simple tension zone models. The inclusion of variation in local vegetation in the model explains a signi®cant proportion of the residual variation in peg number, indicating that habitat-genotype associations contribute to the observed spatial pattern. However, this association is weak, and a number of populations continue to show strong deviations in mean even after habitat is included in the ®nal model. These outliers may be the result of long-distance colonization of sites distant from the cline center or may be due to a patchy pattern of initial contact during postglacial expansion. As well as contrasting with the smooth hybrid zones described for Chorthippus parallelus, this situation also contrasts with the mosaic hybrid zones observed in Gryllus crickets and in parts of the hybrid zone between Bombina toad species, where habitat-genotype associations account for substantial amounts of among-site variation. Key words. Chorthippus, habitat, hybrid zone, long-distance dispersal, mosaic. Received November 21, 2000. Accepted May 21, 2001. Hybrid zones are regions where differentiated genotypes zone, over and above the expectations of tension zone models are broken up by recombination and natural selection acts on (Szymura 1993; MacCallum 1994; MacCallum et al. 1998). the new combinations of alleles generated (Barton 1983; Har- A substantial proportion of these deviations result from hab- rison 1990). The simplest result of this interaction is the itat preference and/or habitat-speci®c selection in an ecolog- formation of a smooth sigmoid cline in allele frequency for ically variable region. The ecological variation maintains each locus, the width of which is determined by a balance high levels of assortative mating even at the center of the between dispersal into the zone and any selection that may hybrid zone, and results in signi®cant associations between be acting against hybrids. Many of the hybrid zones described the mean and variance of a trait in a population and local to date show a close ®t to this model in terms of allele fre- habitat type (MacCallum et al. 1998). quencies at single loci, the distribution of multilocus geno- Habitat-speci®c effects on the distribution of genotypes types through the zone, and the population means of phe- mean that simple models of hybrid zones may not be adequate notypic traits (Barton and Hewitt 1985). predictors of variation in character score along a cline. Hybrid The interaction between dispersal and selection determines zones that show high levels of spatial structure as a result of the widths of clines for independent characters, and the rate genotype-habitat associations have been termed ``mosaic hy- of recombination relative to selection determines the degree brid zones'' by Harrison and Rand (1989). Well-documented to which clines for different characters in¯uence each other's examples of such mosaic hybrid zones include those in Gryl- position and width. For example, in a hybrid zone between lus ground crickets (Harrison and Rand 1989) and Allone- Chorthippus parallelus parallelus and C. parallelus erythro- mobius crickets (Howard 1986). Local habitat has also been pus in the Pyrenees, clines for different morphological and shown to be an important in¯uence on the spatial distributions behavioral characters vary signi®cantly in width and position of different Louisiana Iris species and their respective hybrids (Butlin et al. 1991). In contrast, in hybrid zones between (for review, see Arnold 2000). Such associations may be Bombina toad species, the contribution of many loci to hybrid ®tness seems to restrict how much recombination between caused by differential survival in different habitats (provided loci can occur before selection acts. Developmentally and that patches are suf®ciently large relative to dispersal; Slatkin adaptively distinct quantitative traits therefore show coin- 1973), active habitat preference (MacCallum et al. 1998), or cident clines of similar width (Nurnberger et al. 1995). De- a combination of the two. Both processes reduce recombi- spite this, signi®cant variation between populations in allele nation within the hybrid zone and thus act to maintain local frequencies and levels of linkage disequilibria at ®ve allo- adaptation in the face of gene ¯ow (Cain et al. 1999). zyme loci exist across some transects through the Bombina The study of mosaic hybrid zones allows investigation of the spatial scale at which local adaptation can persist in the face of gene ¯ow and how this is affected by the distribution 2 Present address: The Galton Laboratory, Department of Biol- ogy, Wolfson House, University College London, NW1 2HE, Unit- and nature of the loci that reduce hybrid ®tness. However, ed Kingdom; E-mail: [email protected]. factors other than ecological differentiation can also generate 1832 q 2001 The Society for the Study of Evolution. All rights reserved. SPATIAL STRUCTURE IN A HYBRID ZONE 1833 spatial deviations from a clinal pattern. These include pop- jacobsi are able to ¯y distances of at least 25 m when dis- ulation structure and history, long-distance dispersal, extinc- turbed (pers. obs.) and are rarely found in the lush pastureland tion and recolonization (Nichols 1989), and the possible typical of C. parallelus. Instead, they are common in drier, movement of a cline under selection (Fisher 1937). For ex- ruderal habitats such as roadside verges and dry pasture or ample, the patchy distribution of karyotypes in the Mus do- hay meadows. Species of the Biguttulus group also show mesticus mouse hybrid zone in northern Italy can be explained greater divergence in male calling song than those described by long-distance immigration in foodstuffs imported from for C. parallelus subspecies (Ragge and Reynolds 1998). neighboring areas, following the extinction of local popu- These song differences are known to be important in male lations by ¯ooding (Hauffe and Searle 1993). Such processes mating success and in the ®tness of hybrids (Perdeck 1958; may have important implications for the maintenance and von Helversen and von Helversen 1975). spread of new adaptations by cline movement (Barton and Whitlock 1997; Pialek and Barton 1997) and may signi®- MATERIALS AND METHODS cantly in¯uence the nature of quantitative trait variation available for selection in natural populations. Collection of Males and Morphological Analysis In this study, we ®t a two-dimensional cline to morpho- logical variation across a newly discovered hybrid zone be- A total of 1302 C. brunneus or C. jacobsi males were tween the grasshoppers Chorthippus brunneus (Thunberg) collected from 90 sites across northern Spain during July and and C. jacobsi (Harz) (Orthoptera: Acrididae) in northern August of 1994, 1995, and 1996. According to distribution Spain. The potential of local habitat variation to explain the maps from Ragge et al. (1990), this region was chosen as an observed deviations from ®tted clines is then tested, and pos- area of likely contact between C. brunneus, C. jacobsi, and sible explanations for the structure and position of the hybrid C. yersini. The study area is bounded by the towns of Oviedo zone are discussed in more detail. and San Vicente to the north and Benavente and Palencia to Chorthippus brunneus and C. jacobsi form part of the Bi- the south and includes the Picos de Europa mountain range, guttulus group of Chorthippus (Ragge and Reynolds 1998). which extends almost to the coast of northern Spain. Twenty- Both species are fully winged, although ¯ight is observed two of the sites were visited more than once in subsequent mainly as extended jumps when disturbed. These species are years. In addition, many sites were visited where no C. brun- usually found below 1500 m and have parapatric distributions neus or C. jacobsi individuals were heard, suggesting that the within Europe, which may re¯ect the position of refugia dur- sites sampled represent the full range of habitats inhabited ing the Pleistocene glaciation. Chorthippus brunneus is found by these species in this region. All sites were less than 50 throughout northern Europe, whereas C. jacobsi is restricted m 3 50 m in area and were typically between 5 km and 15 to the Iberian Peninsula. Previous sampling suggested that km apart, although for an intensively studied area at the center these species come into contact in a region close to the Can- of the hybrid zone, most sites were less than 2 km apart. The tabrian Mountains, which form a physical barrier between exact locations of these collection sites are available from northern and central Spain (Ragge and Reynolds 1988). These the authors. They vary in altitude from0mto1450 m above mountains reach altitudes of more than 2500 m in the Picos sea level. de Europa and become lower and more spread out toward Individuals were located within a site by male calling song, the east.