Parallel diversification of Australian gall-thrips on Acacia
Introduction
Evolutionary conservation of associations between plant and phytophagous insect groups is a central theme in biology and provides a platform for testing hypotheses rich in scope (Futuyma and Moreno, 1988, Jermy, 1993, Kelley et al., 2000, Craig et al., 2001, Johnson et al., 2002, Nyman, 2002, Ward et al., 2003, Zerega et al., 2005, Jousselin et al., 2006, McLeish et al., 2007). Coevolution theory (Ehrlich and Raven, 1964) was the historic impetus driving work endeavouring to penetrate factors explaining radiations of both phytophagous insects and their host–plants via selective responses to one another over a relatively long period. ‘Coevolution’ has also been used to demonstrate joint speciation of interacting lineages, or cospeciation (Herre et al., 1996, Clayton et al., 1999, Page, 2003). However, the extent to which phytophagous insects and the plants with which they interact exert selection on one another is complex, highly varied among lineages, and unclear (Jermy, 1984, Jermy, 1993, Ballabeni et al., 2003). In this study, we infer a phylogeny of gall-inducing thrips on Australian Acacia and test hypotheses concerning how this plant–insect assemblage has evolved.
Gall-inducing insects are tightly constrained to mechanisms by which speciation might proceed. Australian gall-inducing thrips are phytophagous insects that have evolved strategies permitting specific utilisation of desert Acacia species for food and shelter and for these reasons gall-induction imposes a level of phylogenetic constraint (Cornell, 1983, Jermy, 1993, Farrell and Mitter, 1998a, Craig et al., 2001, Ward et al., 2003). Host race formation is apparent in gall-thrips on Acacia (Crespi et al., 2004). As well as preadaptation to closely related host plants, cospeciation and host switching across related plants has been shown to result in life history shifts, host specialisation, and the macroevolutionary conservatism in resource use (Ehrlich and Raven, 1964; Berlocher, 2002; Crespi et al., 1998, Crespi et al., 2004, Després and Jaeger, 1999, Cronin and Abrahamson, 2001, Drès and Mallet, 2002, Machado et al., 2005, Rønsted et al., 2005).
Gall-inducing thrips are a monophyletic group that inhabit species of Plurinerves, Juliflorae, and Phyllodinae Acacia subgenera, or sections. Putative gall-thrips species on closely related hosts are of particular interest. Presumably, these taxa have recently diverged and are expected to include taxa near or below species-level and provide a more transparent interpretation of cladogenesis in gall-thrips with fewer extinction events obscuring thrips-Acacia associations. Kladothrips rugosus Froggatt and Kladothrips waterhousei Mound and Crespi induce galls on the same 14 Plurinerves host species showing a high degree of distribution overlap. The phylogenetic relationships among these cryptic taxa are yet to be resolved. Cryptic species are different species that cannot be easily distinguished on the basis of morphology and is indicative of recently diverged species (Jaenike, 1981, Parsons and Shaw, 2001). The apparent cryptic species K. rugosus and K. waterhousei complexes appear overwhelmingly host-specific, they induce disparate taxon-specific gall morphologies, and preliminary molecular work using COI sequence data and microsatellites have provided strong evidence for species-level divergence among them (Mound, 1971, Mound et al., 1996, Crespi et al., 1997, Crespi et al., 1998, McLeish et al., 2006). However, some of these putative species show little genetic divergence, which is suggestive of host race population’s status.
The scope of this work does not include discussion of species definitions, but contends that levels of polymorphism, below that of species, exist in our dataset and require elaboration. Genetic distances among K. rugosus and among K. waterhousei populations show that a large majority of the K. rugosus and K. waterhousei complex members are apparently different species, though additional diagnoses would be useful. Measures of gene flow have to be determined to show reproductive isolation. In addition to genetic distance, it is also crucial to use behavioural and ecological criteria to identify species (Ferguson, 2002). Both the phylogenetic inferences indicate gall structure is highly conserved amongst all newly sampled populations. It is commonly accepted that gall morphology is largely under the control of the insect genome and represents an extended phenotype (Stern, 1995, Crespi and Worobey, 1998, Morris et al., 2002, Stone and Schönrogge, 2003). Fidelity of gall structure over different host species is consistent with gall phenotype being largely determined by the thrips genotype and therefore a potentially useful diagnostic character in species identification. Species-specificity of gall morphology is evident in other insect orders (sawflies: Nyman et al., 2000: wasps: Cook et al., 2002). Recent molecular work (McLeish et al., 2006) has shown two K. rugosus populations, each of which induces a discrete gall type, once believed to be the same species, are different.
The K. rugosus and K. waterhousei complexes thus appear to represent ecological replicates (Johnson and Clayton, 2003) sharing the same set of host species, each expected to cluster into a separate clade and respond in parallel to host speciation via cospeciation, host switching and/or host race formation. These clades thus represent an excellent opportunity to test for parallel diversification and evaluate the roles of historical contingency and selection in evolutionary change (Ricklefs and Schluter, 1993).
Speciation in gall-thrips might proceed by the formation of host-related races where there is reduced gene flow among populations of a single species parasitising two or more localised host species leading to reproductive isolation (Jaenike, 1981, Jaenike, 1990, Emelianov et al., 1995, Parsons and Shaw, 2001, Drès and Mallet, 2002). Speciation via a host-shift can be thought of as a transition from polymorphism (e.g. for host preference) to host race preceding a transition from host race to reproductively isolated species. Host races are maintained by reduced gene flow predominantly via differential host preference. By contrast, host-related sibling species are reproductively isolated for reasons in addition to differential host preference (Jaenike, 1981). Genetic divergence data suggests that host-related races of gall-thrips are actually a series of host specific sibling species, which is consistent with the strong host–plant specificity shown in virtually all other gall-inducing insects (Crespi et al., 2004, Rohfritsch and Shorthouse, 1982).
Cospeciation between phytophagous insects and their hosts, parasites, or mutualists has been clearly demonstrated in a number of cases, most of which involve strong host–plant specificity and intimate insect–plant relationships such as gall-induction or complex physiological and life history adaptation (Ronquist and Nylin, 1990, Baker, 1996, Herre et al., 1996, Machado et al., 1996, Roderick, 1997, Roderick and Metz, 1997, Farrell and Mitter, 1998b, Burckhardt and Basset, 2000, Clark et al., 2000, Itino et al., 2001, Weiblen and Bush, 2002, Weiblen, 2004). The majority of studies, however, indicate that congruence between insect and host plant phylogenies is partial or nonexistent, and thus host-shifting appears to be the more prevalent mechanism in determining the associations of insects and their hosts (Humphries et al., 1986, Weintraub et al., 1995, Janz and Nylin, 1998, Dobler and Farrell, 1999, Janz et al., 2001, Jones, 2001, Lopez-Vaamonde et al., 2001, Ronquist and Liljeblad, 2001). Consequent to host-shifting, fitness tradeoffs between hosts, or ecological divergence of derived, host-shifted populations, may spur the evolution of reproductive isolation (Joshi and Thompson, 1997, Hawthorne and Via, 2001, Nosil et al., 2002), and colonisation of new host–plant lineages may provide opportunities to diversify rapidly (Ehrlich and Raven, 1964, Mitter et al., 1988, Farrell and Mitter, 1998b).
Cospeciation between gall-inducing thrips and host Acacia lineages has been suggested at a macroevolutionary scale in an explicitly phylogenetic context (Crespi et al., 2004). Two thrips lineages, each producing a morphologically discrete elongate or pouched gall type on Acacia sections Plurinerves and Juliflorae can be traced from two ancestral gall-inducing species on a single ancestral Acacia lineage. Both derived thrips lineages have retained the ancestral elongate-pouched gall type combination. A hypothesis of cospeciation makes three predictions (Crespi et al., 2004): (1) phylogenies of parallel thrips lineages should be identical or very similar to each other, (2) phylogenies of thrips lineages should be identical or very similar to that of the host plants, and (3) speciation events among parallel thrips lineages and host lineages should be contemporaneous. Deviations from an identical match would be indicative of processes other than cospeciation operating. Alternatively, the K. rugosus and K. waterhousei groups might have independently converged onto the same set of closely related Acacia conducive to Kladothrips gall-induction, as host-shifts are reported (Craig et al., 1994) to more freely occur among taxonomically and phylogenetically similar plants.
Contradicting the model involving complete cospeciation is evidence that indicates the apparent coincidence in several species of major morphological and life history changes accompanying host switches between more distantly related host lineages that are not inhabited by closely related thrips sister-species (Crespi et al., 2004). These switches are also evidenced by the absence of elongate-pouched gall type combinations and by the presence of only a single gall type on the novel host species, as in Kladothrips intermedius, K. rodwayi and K. morrisi (Crespi et al., 2004). Convergence of thrips lineages among related hosts would predict their phylogenies to be independent of one another. In this paper we test for parallel speciation in the K. rugosus and K. waterhousei species complexes, and evaluate hypotheses for their joint diversification on Australian Acacia. To do so, we first extend and revise the current gall-thrips phylogeny (Morris et al., 2001) with addition of K. rugosus, K. waterhousei, K. habrus, and K. intermedius ‘races’ from different Acacia species; and second, use the phylogeny to test for parallel patterns of diversification between the K. rugsosus and the K. waterhousei groups, which would be indicative of cospeciation of each of these groups with their Acacia hosts, or the parallel evolution of the same set of host–plant shifts.
Section snippets
Collections, DNA extractions, PCR, and sequencing
Taxa were collected from widely distributed Acacia populations across Australia (Table 1). Voucher specimens of these taxa have been deposited in the Australian National Insect Collection (ANIC) at CSIRO Entomology in Canberra. Gall morphology is highly conserved within each gall-thrips taxon with structural diversity exhibited amongst them (Crespi and Worobey, 1998), and was used in conjunction with host species identification (Maslin, 2001) to discriminate amongst gall-thrips races. To test
Results
We extended and revised the phylogeny of Morris et al. (2001) with the inclusion of 16 putative races (on different Acacia species) of the K. rugosus complex and 10 putative races of the K. waterhousei complex that specialise on the same 14 host Acacia species. Maximum parsimony and Bayesian inferences are in general agreement and show a high level of support for each of the clades containing the K. rugosus and K. waterhousei complexes (Fig. 1, Fig. 2). Phylogenetic concordance tests between
Discussion
We inferred phylogenies including numerous undescribed putative species of gall-inducing thrips to test hypotheses of diversification. The addition of these taxa to a previous gall-thrips phylogeny (Morris et al., 2001), results in a tree that includes virtually all known taxonomic entities for this group. A clear pattern has emerged from this expanded tree, suggesting that diversity for this group of specialist insects is generated in close association with host speciation. Maximum parsimony
Acknowledgments
We thank the Evolutionary Biology Unit, South Australia Museum, for their sequencing facilities and technical support. This project was made possible by part funding from the Nature Foundation SA Inc. (Project #7324), the Sir Mark Mitchell Research Foundation (CXS10423800), the Australian Research Council (ARC) to Schwarz M.P., Cooper J.B., Crespi B.J., Chapman T.W., (DP0346322), an ARC Postdoctoral Fellowship to Chapman T.W., and an NSERC grant to Crespi.
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