Phylogeography of the Coccus scale insects inhabiting myrmecophytic Macaranga plants in Southeast Asia

Comparative historical biogeography of multiple symbionts occurring on a common host taxa can shed light on the processes of symbiont diversification. Myrmecophytic Macaranga plants are associated with the obligate mutualistic symbionts: Crematogaster (subgenus Decacrema) ants and Coccus scale insects. We conduct phylogeographic analyses based on mitochondrial cytochrome oxidase I (COI) from 253 scale insects collected from 15 locations in Borneo, Malaya and Sumatra, to investigate the historical biogeography of the scales, and then to draw comparisons with that of the symbiotic, but independently dispersing, Decacrema ants which are not specific to different Coccus lineages. Despite the different mode of ancient diversification, reconstruction of ancestral area and age estimation on the Coccus phylogeny showed that the scales repeatedly migrated between Borneo and Malaya from Pliocene to Pleistocene, which is consistent with the Decacrema ants. Just as with the ants, the highest number of lineages in the scale insects was found in northern northwest Borneo, suggesting that these regions were rainforest refugia during cool dry phases of the Pleistocene. Overall, general congruence between the Plio-Pleistocene diversification histories of the symbiotic scales and ants suggests that they experienced a common history of extinction/migration despite their independent mode of dispersal and host-colonization.ArticlePopulation ecology. 52(1):137-146 (2010)journal articl

Comparative population genetics of mimetic Heliconius butterflies in an endangered habitat; Brazil's Atlantic Forest

<p>Abstract</p> <p>Background</p> <p>Brazil's Atlantic Forest is a biodiversity hotspot endangered by severe habitat degradation and fragmentation. Habitat fragmentation is expected to reduce dispersal among habitat patches resulting in increased genetic differentiation among populations. Here we examined genetic diversity and differentiation among populations of two <it>Heliconius </it>butterfly species in the northern portion of Brazil's Atlantic Forest to estimate the potential impact of habitat fragmentation on population connectivity in butterflies with home-range behavior.</p> <p>Results</p> <p>We generated microsatellite, AFLP and mtDNA sequence data for 136 <it>Heliconius erato </it>specimens from eight collecting locations and 146 <it>H. melpomene </it>specimens from seven locations. Population genetic analyses of the data revealed high levels of genetic diversity in <it>H. erato </it>relative to <it>H. melpomene</it>, widespread genetic differentiation among populations of both species, and no evidence for isolation-by-distance.</p> <p>Conclusions</p> <p>These results are consistent with the hypothesis that the extensive habitat fragmentation along Brazil's Atlantic Forest has reduced dispersal of <it>Heliconius </it>butterflies among neighboring habitat patches. The results also lend support to the observation that fine-scale population genetic structure may be common in <it>Heliconius</it>. If such population structure also exists independent of human activity, and has been common over the evolutionary history of <it>Heliconius </it>butterflies, it may have contributed to the evolution of wing pattern diversity in the genus.</p

FIGURE 2 in Taxonomy of coccids (Hemiptera: Coccidae: Coccus L.) associated with Crematogaster ants (Hymenoptera: Formicidae) in the stems of Macaranga plants (Euphorbiaceae) in Southeast Asia

FIGURE 2. Live coccids and ants inside the cut stems of Macaranga plants: A, C. macarangae Morrison, in M. winkleri, Luasong, Sabah, Borneo (E. Linsenmair, 2003 BF #96); B, C. macarangae, in M. beccariana, Temburong, Brunei, Borneo (P.J. Gullan, PJG-B16); C, C. penangensis Morrison, in M. glandibracteolata, Poring, Sabah, Borneo (B. Fiala, 2003 BF #2); D, C. penangensis, in Macaranga sp., Temburong, Brunei, Borneo (P.J. Gullan, PJG-B31); E, C. pseudotumuliferus Gullan & Kondo sp. n., in M. pearsonii, Tawau, Sabah, Borneo (B. Fiala, 2003 BF #64); F, C. secretus Morrison, in M. indistincta, Tawau, Sabah, Borneo (B. Fiala, 2003 #95). All photographs taken by the collector specified in parentheses.Published as part of Gullan, Penny J., Kondo, Takumasa, Fiala, Brigitte & Quek, Swee-Peck, 2018, Taxonomy of coccids (Hemiptera: Coccidae: Coccus L.) associated with Crematogaster ants (Hymenoptera: Formicidae) in the stems of Macaranga plants (Euphorbiaceae) in Southeast Asia, pp. 1-51 in Zootaxa 4521 (1) on page 10, DOI: 10.11646/zootaxa.4521.1.1, http://zenodo.org/record/377024

Taxonomy of coccids (Hemiptera: Coccidae: Coccus L.) associated with Crematogaster ants (Hymenoptera: Formicidae) in the stems of Macaranga plants (Euphorbiaceae) in Southeast Asia

Gullan, Penny J., Kondo, Takumasa, Fiala, Brigitte, Quek, Swee-Peck (2018): Taxonomy of coccids (Hemiptera: Coccidae: Coccus L.) associated with Crematogaster ants (Hymenoptera: Formicidae) in the stems of Macaranga plants (Euphorbiaceae) in Southeast Asia. Zootaxa 4521 (1): 1-51, DOI: https://doi.org/10.11646/zootaxa.4521.1.

An ancient tripartite symbiosis of plants, ants and scale insects

In the Asian tropics, a conspicuous radiation of Macaranga plants is inhabited by obligately associated Crematogaster ants tending Coccus (Coccidae) scale insects, forming a tripartite symbiosis. Recent phylogenetic studies have shown that the plants and the ants have been codiversifying over the past 16–20 million years (Myr). The prevalence of coccoids in ant–plant mutualisms suggest that they play an important role in the evolution of ant–plant symbioses. To determine whether the scale insects were involved in the evolutionary origin of the mutualism between Macaranga and Crematogaster, we constructed a cytochrome oxidase I (COI) gene phylogeny of the scale insects collected from myrmecophytic Macaranga and estimated their time of origin based on a COI molecular clock. The minimum age of the associated Coccus was estimated to be half that of the ants, at 7–9 Myr, suggesting that they were latecomers in the evolutionary history of the symbiosis. Crematogaster mitochondrial DNA (mtDNA) lineages did not exhibit specificity towards Coccus mtDNA lineages, and the latter was not found to be specific towards Macaranga taxa, suggesting that patterns of associations in the scale insects are dictated by opportunity rather than by specialized adaptations to host plant traits

Nuclear DNA based species delineations of Coccus scale insects in symbiosis with plants and ants, and the role of plant epicuticular wax in structuring associations

We undertook phylogenetic analysis of nuclear DNA to elucidate species boundaries in the symbiotic Coccus scale insects associated with mutualistic Crematogaster ants and Macaranga plants occurring in the ever-wet forests of Southeast Asia. The coccid specimens clustered into ten lineages, each corresponding to a morphospecies assignment. The lineage identified as C. secretus was separated from the Main Clade by an outgroup. We also examined all pairwise associations among the three symbiont guilds to understand how patterns of association were structured. The analyses revealed that each ant, plant or coccid operational (taxonomic) unit often associated with multiple O(T)Us of each of the other two guilds. However, where testing was feasible, a ‘preference’ for one or sometimes two partner O(T)Us of each guild was often detected. Mutual ‘preferences’ or ‘avoidances’ were relatively common among the symbionts, and no conflicts of interest were apparent. The network of preferred partners among all three guilds showed compartmentalization structured by the presence/absence of plant epicuticular wax, suggesting that this feature plays a fundamental role in how the symbionts select partners that best serve their needs. To a lesser degree, the network was also structured by whether the host plant stems were ant-excavated or hollowed naturally.This research was funded by the Japan Ministry of Education, Culture, Sports, Science and Technology (18370010 and 22255001 to TI, 21870012 and 23770018 to SU

Ant List

An Excel spreadsheet listing ant specimens used in the publication, with accompanying information on their mtDNA lineages, locality, host plant, and coccid associate (where present)

Data from: Nuclear DNA based species delineations of Coccus scale insects in symbiosis with plants and ants, and the role of plant epicuticular wax in structuring associations

We undertook phylogenetic analysis of nuclear DNA to elucidate species boundaries in the symbiotic Coccus scale insects associated with mutualistic Crematogaster ants and Macaranga plants occurring in the ever-wet forests of Southeast Asia. The coccid specimens clustered into ten lineages, each corresponding to a morphospecies assignment. The lineage identified as C. secretus was separated from the Main Clade by an outgroup. We also examined all pairwise associations among the three symbiont guilds to understand how patterns of association were structured. The analyses revealed that each ant, plant or coccid operational (taxonomic) unit often associated with multiple O(T)Us of each of the other two guilds. However, where testing was feasible, a ‘preference’ for one or sometimes two partner O(T)Us of each guild was often detected. Mutual ‘preferences’ or ‘avoidances’ were relatively common among the symbionts, and no conflicts of interest were apparent. The network of preferred partners among all three guilds showed compartmentalization structured by the presence/absence of plant epicuticular wax, suggesting that this feature plays a fundamental role in how the symbionts select partners that best serve their needs. To a lesser degree, the network was also structured by whether the host plant stems were ant-excavated or hollowed naturally

Coccus list Table S1

An Excel spreadsheet listing all Coccus specimens used for the publication, their morphospecies assignments and nuclear DNA clade, and including information on their host plants, host ants, and location