Gall-induction in insects: evolutionary dead-end or speciation driver?
Nate B Hardy
1
Lyn G Cook
0
0
The University of Queensland, School of Biological Sciences
,
Brisbane, Queensland 4072
,
Australia
1
Queensland Primary Industries and Fisheries
,
Entomology, Brisbane, Queensland 4068
,
Australia
Background: The tree of life is significantly asymmetrical - a result of differential speciation and extinction - but general causes of such asymmetry are unclear. Differences in niche partitioning are thought to be one possible general explanation. Ecological specialization might lead to increases in diversification rate or, alternatively, specialization might limit the evolutionary potential of specialist lineages and increase their extinction risk. Here we compare the diversification rates of gall-inducing and non-galling insect lineages. Compared with other insect herbivores feeding on the same host plant, gall-inducing insects feed on plant tissue that is more nutritious and less defended, and they do so in a favorable microhabitat that may also provide some protection from natural enemies. We use sister-taxon comparisons to test whether gall-inducing lineages are more host-specific than non-galling lineages, and more or less diverse than non-gallers. We evaluate the significance of diversity bipartitions under Equal Rates Markov models, and use maximum likelihood model-fitting to test for shifts in diversification rates. Results: We find that, although gall-inducing insect groups are more host-specific than their non-galling relatives, there is no general significant increase in diversification rate in gallers. However, gallers are found at both extremes - two gall-inducing lineages are exceptionally diverse (Euurina sawflies on Salicaceae and Apiomorpha scale insects on Eucalytpus), and one gall-inducing lineage is exceptionally species-poor (Maskellia armored scales on Eucalyptus). Conclusions: The effect of ecological specialization on diversification rates is complex in the case of gall-inducing insects, but host range may be an important factor. When a gall-inducing lineage has a host range approximate to that of its non-galling sister, the gallers are more diverse. When the non-galler clade has a much wider host range than the galler, the non-galler is also much more diverse. There are also lineage-specific effects, with gallers on the same host group exhibiting very different diversities. No single general model explains the observed pattern.
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Background
The tree of life is significantly less balanced than
expected under a stochastic process of lineage
divergence and extinction [1] - some lineages are diverse
whereas others are species-poor. Deterministic
explanations for the asymmetry include clade age [2], and
among-lineage diversification rate variation [3] caused
by mass extinction [4], lineage attributes [5-9],
environmental attributes [10,11], and ecosystem attributes
[12,13] (Figure 1). Lineage attributes affecting
diversification rates can be divided into two classes: (1)
phenotypic traits that are attributes of individuals, for example
reproductive rate, dispersal ability, and the degree of
* Correspondence:
1Queensland Primary Industries and Fisheries, Entomology, Brisbane,
Queensland 4068, Australia
Full list of author information is available at the end of the article
ecological specialization; and (2) traits that are attributes
of species, for example geographic range, population
size, and local abundance. A key factor in the theory of
diversification rate variation is resource availability and
breadth, i.e. adaptive zone dimensions. Under an
adaptive radiation model [14-16] it is argued that
diversification is limited to the amount of free space in an
adaptive zone, and that elevated rates of diversification
are driven by ecological opportunities in geographic
space (e.g. island colonization) or the evolution of an
adaptive trait (key innovation). Well-studied examples of
adaptive radiation include the Hawaiian silverswords
[17], phytophagous beetles [12,18], and columbines [16].
Ecological specialization is thought to be an important
process following expansion of a lineages adaptive zone,
and a major driving force generating species richness
and diversity [15,19-21].
+ ERM models1
mass extinction4
phylogeny
imbalance
among-lineage
diversification
rate variation3
+ geographic range8
+ population size8
+ abundance9
+ productivity11
+ geologic boundary
distribution11
+ adaptive zone
dimensions13,14
Figure 1 Classification of causes of tree imbalance. Examples of attributes that are commonly discussed in the literature are preceded by +,
with references in superscript. Mass extinction is shown as both random and deterministic; mass extinctions are stochastic events, but not the
type captured by purely neutral ERM models.
Not all adaptive traits are expected to result in an
increased rate of net diversification; on the contrary,
some adaptive traits may result in a dramatic depression
of the diversification rate e.g. in-bred sociality in
theridiid spide (...truncated)