Older Lineages of Oribatid Mites in Mountain Ranges Have Broader Geographic Ranges and Exhibit More Generalistic Traits

Abstract

Understanding ecological and evolutionary mechanisms that drive biodiversity patterns is important for comprehending biodiversity. Despite being critically important to the functioning of ecosystems, the mechanisms driving belowground biodiversity are little understood. We investigated the radiation and trait diversity of soil oribatid mites from two mountain ranges, that is, the Alps in Austria and Changbai Mountain in China, at similar latitude in the temperate zone differing in formation processes (orogenesis) and exposed to different climates. We collected and sequenced soil oribatid mites from forests at 950-1700 m at each mountain and embedded them into the chronogram of species from temperate Eurasia. We investigated the phylogenetic age of oribatid mites and compared the node age of species with the mountain uplift time of the Alps and Changbai Mountain. We then inspected trophic variation, geographical range size, and reproductive mode, and identified traits that promote oribatid mite survival and evolution in montane forest ecosystems. We found that oribatid mites on Changbai Mountain are phylogenetically older than species in the Alps. All species on Changbai Mountain evolved long before the uplift of Changbai Mountain, but some species in the Alps evolved after the orogenesis of the Alps. On Changbai Mountain, more species possess broader trophic variation, have larger geographical range sizes, and more often reproduce via parthenogenesis compared to species from the Alps. Species on Changbai Mountain survived the mountain uplift or colonized the mountain thereafter, supporting the view that generalistic traits promote survival and evolution in phylogenetically old soil animal species. Collectively, our findings highlight that combining species traits and phylogeny allow deeper insight into the evolutionary forces shaping soil biodiversity in montane ecosystems.

Keywords: biogeography; geographic range size; mountains; oribatid mites; reproductive mode; trophic niche.

FIGURE 1

Geographic position, orogenesis, the extend of Quaternary glaciation of the study sites and sampling locations along the studied altitudinal gradients spanning from 950 to 1700 m in the Alps (Austria) and on Changbai Mountain (China). Alps was formed gradually after a series of continental plate collisions (a) while Changbai Mountain was formed gradually after a series of volcanic eruptions (b). The main stage of mountain uplift was 99.6–23.0 mya in the Alps and 22.6–0.01 mya on Changbai Mountain. Both mountains experienced the Quaternary glaciation with the light blue area representing the extent of permafrost in the Eurasia during the Last Permafrost Maximum (Vandenberghe et al. 2014).

FIGURE 2

Phylogeny and traits (reproductive mode, trophic variation and range size) of oribatid mites from the Alps (28 species) and Changbai Mountain (20 species), embedded into the chronogram of the oribatid mite species from the Eurasian continent (76 species). Amblyomma boeroi , Allothyrus sp., and Opilioacarus texanus (Acari: Parasitiformes) are used as outgroups. The phylogeny is based on 18S rDNA sequences. Numbers on black circles show the distribution of nodes with species known from the fossil record that were used as priors in the molecular clock analysis ((1) oribatid mites, 407–385 mya, (2) Protoplophoridae, 336–326 mya, (3) Hypochthoniidae, 336–326 mya, (4) Cosmochthoniidae, 336–326 mya, (5) Trhypochthoniidae, 112–99 mya, (6) Trhypochthoniidae, 151–146 mya, (7) Oppiidae, 28–23 mya, (8) Oribatulidae, 49–40 mya; for details and references see Table 2). The red block indicates the main stage of mountain uplift in the Alps (99.6–23.0 mya), the green block indicates the main stage of mountain uplift on the Changbai Mountain (22.6–0.01 mya). The red, green, and purple triangles represent the oribatid mite species in the Alps, on Changbai Mountainand at both of the two mountains, respectively. The orange and blue circles represent parthenogenetic and sexual oribatid mite species, respectively. The brown and green circles represent trophic variation (calculated based on standard deviation in Δ15N values; for details see Section 2 and Table S4) and known geographical range size of oribatid mite species, with the size of circles representing the degree of trophic variation and the size of the geographical range size.

FIGURE 3

Distribution of the null expectation of randomized mean pairwise distance (MPD) of oribatid mite divergence estimate for the Alps (a) and Changbai Mountain (b). The red and green vertical lines represent the observed MPD for the Alps (514 mya) and Changbai Mountain (577 mya), respectively; for details see text.

FIGURE 4

Trophic variation (a) and geographical range size (b) of oribatid mite species from the Alps and Changbai Mountain. The box plots include mean (rhombic symbol), median (horizontal line), and interquartile range (box); error bars represent 95% confidence intervals. Each point represents one species. Asterisks indicate significant effects, with *p < 0.05 and ***p < 0.001.