Evolution of a key trait greatly affects underground community assembly process through habitat adaptation in earthworms

Abstract

Underground community assemblies have not been studied well compared with aboveground communities, despite their importance for our understanding of whole ecosystems. To investigate underground community assembly over evolutionary timescales, we examined terrestrial earthworm communities (Oligochaeta: Haplotaxida) in conserved mountainous primary forests in Japan as a model system. We collected 553 earthworms mostly from two dominant families, the Megascolecidae and the Lumbricidae, from 12 sites. We constructed a molecular taxonomic unit tree based on the analysis of three genes to examine the effects of a biogeographic factor (dispersal ability) and an evolutionary factor (habitat adaptation) on the earthworm community assembly process. The phylogenetic distance of the earthworm communities among sites was positively correlated with geographic distance when intraspecific variation was included, indicating that the divergence within species was affected by biogeographic factors. The community assembly process in the Megascolecidae has also been affected by environmental conditions in relation to an evolutionary relationship between habitat environment and intestinal cecum type, a trait closely related to habitat depth and diet, whereas that in the Lumbricidae has not been affected as such. Intestinal cecum type showed a pattern of niche conservatism in the Megascolecidae lineage. Our results suggest that investigating the evolution of a key trait related to life history can lead to the clear description of community assembly process over a long timescale and that the community assembly process can differ greatly among related lineages even though they live sympatrically.

Pontoscolex corethrurus: A homeless invasive tropical earthworm?

“…This suggests that P . corethrurus consumes and degrades a greater variety of organic materials given its greater ability (efficiency), evidenced by: a) producing endogenous cellulases [59–62]; b) its association with the gut microbiota [63–66]; c) gene expression (transcriptome) that contribute to the adaptation of its digestive system [65]; d) improving its digestion efficiency according to the type of cecum [59, 67]; and e) its association with nephridial bacteria [50, 68, 69].…”

A comparison of latitudinal species diversity patterns between riverine and terrestrial earthworms from the North American temperate zone

“…The total genomic DNA of earthworms was extracted using DNeasy Blood & Tissue Kit (Qiagen). The following primers were used for PCR amplification and direct sequencing: mitochondrial COI gene: LCO1490 (forward), 5′-GGT CAA CAA ATC ATA AAG ATA TTG G-3′ (Folmer, Black, Hoeh, Lutz, & Virjenhoek, 1994) (forward), 5′-CCT AGG AGT CGG GTT GTT TG-3′ (this study), 28SD3 (forward), 5′-GAG TCG GGT TGT TTG AGA TTG-3′ (this study), 28s-rD5b (reverse), 5′-CCA CAG CGC CAG TTC TGC TTA C-3′ (Whiting., 2002); and nuclear H3 gene: H3F (forward), 5′-ATG GCT CGT ACC AAG CAG ACV GC-3′ (Colgan et al, 1998), H3R (reverse), 5′-ATA TCC TTR GGC ATR ATR GTG AC-3′ (Colgan et al, 1998), H3R4 (reverse), 5′-TGG GCA TGA TGG TGA CGC GCT-3′ (Ikeda et al, 2018). Sequencing of the purified PCR products was performed using the services of Macrogen.…”

“…We split the potential species (molecular operational taxonomic units: MOTUs) from the phylogenetic trees that include divergence within species (haplotype tree) because morphological identification of earthworms is difficult and relies on a relatively small number of characters, including sexual characters that may or may not be fully developed at the time of collection (e.g. Ikeda et al, 2018;Ikeda et al, 2012). Species-level classification of Sparganophilus has also not been well-studied and is currently in development (Carerra-Martínez, 2018).…”

“…However, it is difficult to identify earthworm species using their morphological characters because these external morphological characters are relatively limited in number and depend on the full development of sexual characters in individual specimens (e.g. Ikeda et al, 2018;Ikeda, Tsuchiya, Nagata, Ito, & Sota, 2012). Species-level classification of the genus Sparganophilus has not been seriously pursued since the 1970s, but more work in this area is expected to reveal many more species than currently described (Carerra-Martínez, 2018).…”

“…Species-level classification of the genus Sparganophilus has not been seriously pursued since the 1970s, but more work in this area is expected to reveal many more species than currently described (Carerra-Martínez, 2018). Fortunately, in the light of the difficulty in identifying specimens, it has become an increasingly accepted practice in recent years to use molecular designations of species identity to allow previously unidentifiable specimens to be used in ecological studies (Ikeda et al, 2018;Richard et al, 2010).…”