Guy L. Bush

SYMPATRIC HOST RACE FORMATION AND SPECIATION IN FRUGIVOROUS FLIES OF THE GENUS RHAGOLETIS (DIPTERA, TEPHRITIDAE)

The origin and evolution of species and host racesl in certain phytophagous insect groups have long been a source of disagreement among evolutionary biologists. The rapid establishment of new host races by some stenophagous insects on introduced plants, as well as various other aspects of their biology and distribution, has led several biologists to suggest that new host races and species may arise sympatrically (Brues, 1924; Thorpe, 1930; Smith, 1941; Haldane, 1959; Alexander and Bigelow, 1960; Bush, 1966). Others regard geographic isolation as a prerequisite for speciation in all groups of sexually reproducing animals (for examples see Mayr, 1963). The difficulty in resolving whether either one or the other, or both, modes of speciation may occur in these insects stems directly from the paucity of detailed studies of wild stenophagous insects. Our information on these insects has been derived primarily from studies made over the past hundred years on a few economically important plant pests. One such group that has received particular attention is the Holarctic and Neotropical genus Rhagoletis whose larvae feed within the developing fruits of many plant species such as cherries, blueberries, apples, currants, rose hips, walnuts, and tomatoes. The objective of this paper is to point out how the biological attributes of these flies may have permitted new forms to arise rapidly in the absence of geographical barriers to gene flow.

Sympatric speciation in animals: new wine in old bottles

Recent research on natural host races and sympatric sister species, comparative phylogenetic analyses, laboratory experiments and theoretical models has greatly strengthened the case for sympatric speciation. Traits evolving in response to divergent selection experienced by subpopulations adapting to different habitats provide sufficient intrinsic premating isolation for sympatric speciation to occur. The initiation of speciation through a habitat shift in animals which mate within a preferred habitat (such as many phytophagous and parasitic invertebrates and some vertebrates, including birds) requires few genetic changes.

Sympatric Speciation in Phytophagous Parasitic Insects

The appearance of new insect pests on economically important plants is a well-known phenomenon to many applied biologists. In addition, populations of introduced or native insects are frequently encountered which exhibit different host preferences, but which are morphologically indistinguishable from one another (Brues 1924, Simms 1931, Mayr 1942, Andrewartha and Birch 1954, Zwolfer and Harris 1971). These so-called host races sometimes actually represent previously unrecognized reproductively isolated sibling species. Others appear to retain their distinct host preferences and other biological traits in the absence of any observable barriers to gene flow between the races. Two classic examples in North America are the codling moth (Laspeyresia pomonella), introduced from Europe in 1750, which shifted from apples to walnuts about 26 years after it reached California in 1873 (Essig 1931, Foster 1912), and the apple maggot (Rhagoletis pomonella) which moved from its native host hawthorn to introduced apples in 1864 and cherries less than 20 years ago (Bush 1966, 1969a,b, 1974).

Conditions for sympatric speciation: A diploid model incorporating habitat fidelity and non-habitat assortative mating

SummaryThree types of genes have been proposed to promote sympatric speciation: habitat preference genes, assortative mating genes and habitat-based fitness genes. Previous computer models have analysed these genes separately or in pairs. In this paper we describe a multilocus model in which genes of all three types are considered simultaneously. Our computer simulations show that speciation occurs in complete sympatry under a broad range of conditions. The process includes an initial diversification phase during which a slight amount of divergence occurs, a quasi-equilibrium phase of stasis during which little or no detectable divergence occurs and a completion phase during which divergence is dramatic and gene flow between diverging habitat morphs is rapidly eliminated. Habitat preference genes and habitat-specific fitness genes become associated when assortative mating occurs due to habitat preference, but interbreeding between individuals adapted to different habitats occurs unless habitat preference is almost error free. However, ‘nonhabitat assortative mating’, when coupled with habitat preference can eliminate this interbreeding. Even when several loci contribute to the probability of expression of non-habitat assortative mating and the contributions of individual loci are small, gene flow between diverging portions of the population can terminate within less than 1000 generations.

Speciation in fig pollinators and parasites.

Here we draw on phylogenies of figs and fig wasps to suggest how modes of speciation may be affected by interspecific interactions. Mutualists appear to have cospeciated with their hosts to a greater extent than parasites, which showed evidence of host shifting. However, we also repeatedly encountered a pattern not explained by either cospeciation or host switching. Sister species of fig parasites often attack the same host in sympatry, and differences in ovipositor length suggest that parasite speciation could result from divergence in the timing of oviposition with respect to fig development. These observations on fig parasites are consistent with a neglected model of sympatric speciation.

THE GENETICS OF HOST SELECTION AND ITS BEARING ON SYMPATRIC SPECIATION IN PROCECIDOCHARES (DIPTERA: TEPHRITIDAE)

The genetics of host selection, in terms of oviposition behavior, was investigated in two species of monophagous gall‐forming flies. The existence of a single major allele difference in the genetic basis of host selection was established by a series of hybrid crosses between these flies. The complimentary role of conditioning was also investigated. The apparently simple genetic change required to produce a change in host selection suggests a mechanism of sympatric speciation applicable to these insects.

The genetics and ecology of sympatric speciation: a case study

Mating occurs on the larval host plant in allRhagoletis species (Diptera: Tephritidae). We show how this attribute, when coupled with certain differences in other biological traits, strongly influences the mode of speciation. In species of thesuavis species group, host shifts have never occurred during speciation, and larvae feed in the husks of any walnut species(Juglans spp.), which are highly toxic. Taxa are allopatric or parapatric and exhibit deep phylogenetic nodes suggesting relatively ancient speciation events. Traits responsible for species and mate recognition, particularly in parapatric species, are morphologically distinct and strongly sexually dimorphic. All aspects of their biology, genetics and distribution are consistent with a slow rate of allopatric speciation followed by morphological divergence in secondary contact. In contrast, speciation in thepomonella species group has always involved a shift to a new, usually unrelated, non-toxic host, and all taxa within these groups are sympatric, monophagous and morphologically indistinguishable from one another. Phylogenetic nodes are very shallow, indicating recent sympatric speciation. Sympatric divergence is promoted by genetic variation which allows a portion of the original species to shift to a new habitat or host. Evidence suggests that changes in a few key loci responsible for host selection and fitness on a new host may initiate host shifts. By exploiting different habitats, competition for resources between diverging populations is reduced or avoided. We provide evidence that in phytophagous and parasitic insects sufficient intrinsic barriers to gene flow can evolve between sister populations as they adapt to different habitats or hosts to allow each population to establish independent evolutionary lineages in sympatry.

A field test of differential host-plant usage between two sibling species of Rhagoletis pomonella fruit flies (Diptera-Tephritidae) and its consequences for sympatric models of speciation

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Gene frequency clines for host races of Rhagoletis pomonella in the midwestern United States

Speciation in many host specific parasites may be initiated in sympatry when populations shift and adapt to new hosts. The recent shift of the apple maggot fly, Rhagoletis pomonella (Diptera: Tephritidae) from its native host plant hawthorn (Crataegus spp.) to introduced, domesticated apple (Malus pumila), provides a direct test of the “sympatric speciation” hypothesis by indicating whether partially reproductively isolated “host races” can evolve in the absence of geographic isolation. We report finding significant allele frequency differences for six allozymes between paired apple and hawthorn infesting populations of R. pomonella from across the midwestern United States. Latitudinal allele frequency clines exist among both apple and hawthorn populations, however, for a majority of the loci displaying racial differences. Inter-host genetic differentiation is therefore superimposed on clinal patterns of variation within the races such that the magnitude of host associated divergence is a function of latitude. The results indicate that host associated races can form in sympatry and implicate differences in host plant recognition and developmental timing (related to ambient temperature) as key factors restricting gene flow between apple and hawthorn populations. However, some of the same processes differentiating apple and hawthorn populations at sympatric sites also appear to be occurring within the two host races across their respective ranges. R. pomonella populations are therefore diverging with respect to both their host plant affiliations and local environmental conditions.

The evolutionary significance of bacteria associated with Rhagoletis

All Rhagoletis reportedly establish associations with one or more bacterial species, but the bases for these interactions and their implications for host race formation and speciation are poorly understood. Here we present the results of four studies designed to increase our understanding of these relationships. In the first study, we identify the bacteria associated with seven Rhagoletis taxa by surveying the inhabitants of the esophageal bulb, an organ whose major function appears to be the housing of microorganisms. The results suggest that no bacterium has entered into an obligate symbiotic relationship with any of the Rhagoletis taxa surveyed, although one bacterium, Klebsiella oxytoca, is a very common associate of six of the seven. In the second study we use horizontal starch gel electrophoresis to determine the genetic similarity of K. oxytoca clones isolated from different Rhagoletis populations. This analysis provides a rare look into the genetic structure of natural populations of an enteric bacterium and permits the construction of a dendrogram for the clones—a dendrogram which indicates that there is no clear‐cut pattern to the distribution of K. oxytoca genotypes among Rhagoletis. Taken together, the above studies provide indirect evidence that the bacteria associated with Rhagoletis are not important determinants of host plant specificity. The third and fourth studies assess two possible functions associated bacteria may perform for Rhagoletis: pectic substances degradation and nitrogen fixation. Our results do not lend support to either function.