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Phylogenetic test of speciation by host shift in leaf cone moths ( Caloptilia ) feeding on maples ( Acer )

View Article: PubMed Central - PubMed

ABSTRACT

The traditional explanation for the exceptional diversity of herbivorous insects emphasizes host shift as the major driver of speciation. However, phylogenetic studies have often demonstrated widespread host plant conservatism by insect herbivores, calling into question the prevalence of speciation by host shift to distantly related plants. A limitation of previous phylogenetic studies is that host plants were defined at the family or genus level; thus, it was unclear whether host shifts predominate at a finer taxonomic scale. The lack of a statistical approach to test the hypothesis of host‐shift‐driven speciation also hindered studies at the species level. Here, we analyze the radiation of leaf cone moths (Caloptilia) associated with maples (Acer) using a newly developed, phylogeny‐based method that tests the role of host shift in speciation. This method has the advantage of not requiring complete taxon sampling from an entire radiation. Based on 254 host plant records for 14 Caloptilia species collected at 73 sites in Japan, we show that major dietary changes are more concentrated toward the root of the phylogeny, with host shift playing a minor role in recent speciation. We suggest that there may be other roles for host shift in promoting herbivorous insect diversification rather than facilitating speciation per se.

No MeSH data available.


Phylogenetic distributions of host use arising from different speciation modes in herbivorous insects. (A) Distribution of host use on the phylogeny of a hypothetical insect group in which speciation is mainly associated with host shifts. (B) Distribution of host taxa when speciation mainly involves other processes without host shifts.
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ece32266-fig-0002: Phylogenetic distributions of host use arising from different speciation modes in herbivorous insects. (A) Distribution of host use on the phylogeny of a hypothetical insect group in which speciation is mainly associated with host shifts. (B) Distribution of host taxa when speciation mainly involves other processes without host shifts.

Mentions: In this study, we assess the importance of host shifts in the speciation process of herbivorous insects by developing a new method that overcomes these issues. This method focuses on whether host plant shifts are concentrated toward the roots or the tips of the insect phylogenetic tree, while taking into account host plant phylogeny in the calculation of host use dissimilarity between a pair of herbivorous insect species. If most speciation events are associated with host shifts, the level of disparity in host use between a pair of herbivorous insect species will on average be greater for phylogenetically more closely related pairs (Fig. 2A). Alternatively, if most host shifting events occurred during the initial stage of the radiation and more recent speciation events were independent of host shifts, the level of difference in host use would be larger toward the root of the phylogenetic tree (Fig. 2B). We focused on the interaction between a group of leaf cone moths (Caloptilia, Gracillariidae) and their maple hosts (Acer, Sapindaceae). The Caloptilia–Acer interaction is appropriate for testing host‐shift‐driven speciation at fine taxonomic scales because a previous study demonstrated large variation in the pattern of host use among Caloptilia species (Nakadai and Murakami 2015). The genus Acer is one of the most taxonomically diverse groups of trees in the Northern Hemisphere, particularly in the temperate regions of East Asia, eastern North America, and Europe (van Gelderen et al. 1994). The genus comprises 124 species in the Northern Hemisphere, 81% of which are distributed in China, Korea, and Japan (Renner et al. 2007). A previous taxonomic study of Caloptilia identified 11 species associated with Acer in Japan alone, which have high morphological affinity to each other (Kumata 1982). Based on extensive geographic sampling, we establish full host plant records for these 11 species and three newly found ones, and analyze them using the above method to assess the relative importance of host shift in the speciation of Caloptilia moths feeding on Acer trees.


Phylogenetic test of speciation by host shift in leaf cone moths ( Caloptilia ) feeding on maples ( Acer )
Phylogenetic distributions of host use arising from different speciation modes in herbivorous insects. (A) Distribution of host use on the phylogeny of a hypothetical insect group in which speciation is mainly associated with host shifts. (B) Distribution of host taxa when speciation mainly involves other processes without host shifts.
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Related In: Results  -  Collection

License
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getmorefigures.php?uid=PMC4979720&req=5

ece32266-fig-0002: Phylogenetic distributions of host use arising from different speciation modes in herbivorous insects. (A) Distribution of host use on the phylogeny of a hypothetical insect group in which speciation is mainly associated with host shifts. (B) Distribution of host taxa when speciation mainly involves other processes without host shifts.
Mentions: In this study, we assess the importance of host shifts in the speciation process of herbivorous insects by developing a new method that overcomes these issues. This method focuses on whether host plant shifts are concentrated toward the roots or the tips of the insect phylogenetic tree, while taking into account host plant phylogeny in the calculation of host use dissimilarity between a pair of herbivorous insect species. If most speciation events are associated with host shifts, the level of disparity in host use between a pair of herbivorous insect species will on average be greater for phylogenetically more closely related pairs (Fig. 2A). Alternatively, if most host shifting events occurred during the initial stage of the radiation and more recent speciation events were independent of host shifts, the level of difference in host use would be larger toward the root of the phylogenetic tree (Fig. 2B). We focused on the interaction between a group of leaf cone moths (Caloptilia, Gracillariidae) and their maple hosts (Acer, Sapindaceae). The Caloptilia–Acer interaction is appropriate for testing host‐shift‐driven speciation at fine taxonomic scales because a previous study demonstrated large variation in the pattern of host use among Caloptilia species (Nakadai and Murakami 2015). The genus Acer is one of the most taxonomically diverse groups of trees in the Northern Hemisphere, particularly in the temperate regions of East Asia, eastern North America, and Europe (van Gelderen et al. 1994). The genus comprises 124 species in the Northern Hemisphere, 81% of which are distributed in China, Korea, and Japan (Renner et al. 2007). A previous taxonomic study of Caloptilia identified 11 species associated with Acer in Japan alone, which have high morphological affinity to each other (Kumata 1982). Based on extensive geographic sampling, we establish full host plant records for these 11 species and three newly found ones, and analyze them using the above method to assess the relative importance of host shift in the speciation of Caloptilia moths feeding on Acer trees.

View Article: PubMed Central - PubMed

ABSTRACT

The traditional explanation for the exceptional diversity of herbivorous insects emphasizes host shift as the major driver of speciation. However, phylogenetic studies have often demonstrated widespread host plant conservatism by insect herbivores, calling into question the prevalence of speciation by host shift to distantly related plants. A limitation of previous phylogenetic studies is that host plants were defined at the family or genus level; thus, it was unclear whether host shifts predominate at a finer taxonomic scale. The lack of a statistical approach to test the hypothesis of host‐shift‐driven speciation also hindered studies at the species level. Here, we analyze the radiation of leaf cone moths (Caloptilia) associated with maples (Acer) using a newly developed, phylogeny‐based method that tests the role of host shift in speciation. This method has the advantage of not requiring complete taxon sampling from an entire radiation. Based on 254 host plant records for 14 Caloptilia species collected at 73 sites in Japan, we show that major dietary changes are more concentrated toward the root of the phylogeny, with host shift playing a minor role in recent speciation. We suggest that there may be other roles for host shift in promoting herbivorous insect diversification rather than facilitating speciation per se.

No MeSH data available.