Systematics and biogeography of the subgenus Heteromurus (Verhoeffiella) (Collembola: Entomobryidae) in the Dinaric Karst

Lukić, Marko (author), Zagmajster, Maja (mentor), Deharveng, Louis (co-mentor)

We explored evolutionary pathways and diversification in subterranean environments using the collembolan cave genus Verhoeffiella (formerly a subgenus of Heteromurus) as a study model. We conducted thorough morphological analyses of Verhoeffiella, tested the monophyly of the genus, explored its relationship with putative surface relative Heteromurus nitidus, and its temporal patterns of molecular diversification. The basis of the study were 411 individuals collected from 105 sites, throughout the Verhoeffiella distributional range (Iberian Peninsula, the Alps, Dinarides). We have set up a morphological framework for describing species of Verhoeffiella and found new taxonomically relevant diagnostic characters. Based on our work, the number of described species rose from 9 to 14 species. Molecular phylogeny showed that the genera Verhoeffiella and Heteromurus form a clade nested within Heteromurinae. Within the clade, both Verhoeffiella and Heteromurus were not monophyletic, implicating the need for taxonomic re-arrangements at the generic level of Heteromurinae. Molecular species delimitation methods disclosed remarkable diversification of Verhoeffiella within Dinarides, where a complex geographical pattern of five Verhoeffiella lineages resulted in a high number of co‐occurring molecular operational taxonomic units. Divergence time estimation showed two boosts of diversification, one linked to the Messinian salinity crisis and the other to Pleistocene climatic oscillations. The discovery of extensive subterranean diversification of Verhoeffiella and its closely related epigean relative Heteromurus nitidus makes Verhoeffiella a model of utmost interest within the subterranean fauna of temperate areas, where the phylogenetic origin of most troglobiotic taxa remain poorly known.

• Language: English
• Keywords: chaetotaxy, troglomorphy, troglobionts, cryptic diversity, disjunct distribution, Collembola, Pleistocene, Messinian salinity crisis, Dinaric Karst
• Work type: Doctoral dissertation
• Typology: 2.08 - Doctoral Dissertation
• Organization: BF - Biotechnical Faculty
• Year: 2020
• PID: 20.500.12556/RUL-116070
• COBISS.SI-ID: 22877699
• Publication date in RUL: 13.05.2020

Secondary language

• Language: Slovenian
• Title: Sistematika in biogeografija podrodu Heteromurus (Verhoeffiella) (Collembola: Entomobryidae) na Dinarskem krasu

Abstract

Raziskovali smo evolucijske poti in diverzifikacijo v podzemnih habitatih, pri čemer smo za študijski model uporabili podzemni rod skakačev Verhoeffiella (prej podrod rodu Heteromurus). Naredili smo podrobno morfološko študijo rodu Verhoeffiella, testirali monofilijo rodu, raziskali njegov odnos z domnevnim površinskim sorodnikom Heteromurus nitidus, in časovne vzorce molekulske diverzifikacije. Osnova študije je bil nabor 411 osebkov, ki so bili nabrani na 105 lokalitetah po območju razširjenosti rodu Verhoeffiella (Iberski polotok, Alpe, Dinaridi). Pripravili smo morfološki okvir za opisovanje vrst Verhoeffiella in našli nove razločevalne znake. Na podlagi našega dela je število opisanih vrst naraslo z 9 na 14 vrst. Molekulska filogenija je pokazala, da tvorita rodova Verhoeffiella in Heteromurus klad znotraj Heteromurinae. Znotraj klada pa noben od teh dveh rodov ni monofiletski, ki naazujejo da bodo potrebne taksonomske spremembe na rodovnem nivoju znotraj Heteromurinae. Molekulska delimitacija vrst je razkrila izjemno diverzifikacijo rodu Verhoeffiella znotraj Dinaridov, kjer se je pokazal kompleksen geografski vzorec petih linij z velikim številom sopojavljajočih se molekulskih operacijskih taksonomskih enot. Ocena časovne divergence je pokazala dva vrhova diverzifikacije, enega povezanega z Mesinijsko slanostno krizo, drugega pa s pleistocenskimi klimatskimi nihanji. Odkritje obsežne podzemne diverzifikacije rodu Verhoeffiella in bližnjega površinskega sorodnika Heteromurus nitidus postavlja rod Verhoeffiella na posebno zanimivo mesto znotraj podzemne favne zmernih klimatov, kjer je filogenetski izvor številnih troglobiotskih taksonov slabo poznan.

• Keywords: hetotaksija, troglomorfije, troglobionti, kriptična diverziteta, disjunktna razširjenost, Collembola, plestocen, Mesinijska slanostna kriza, Dinaridi