Addressing the Linnean shortfall in a cryptic species complex

Abstract

Biodiversity is being lost at an alarming rate, but the rate of this loss is likely to be underestimated as a result of a deficit in taxonomic knowledge (i.e. the Linnean shortfall). This knowledge gap is more extensive for morphologically indistinct taxa. The advancement of molecular techniques and delimitation methods has facilitated the identification of such cryptic species, but a majority of these taxa remain undescribed. To investigate the effects of taxonomic uncertainty on understanding of biodiversity, we applied the general lineage concept of species to an amphipod species complex, the Gammaruslacustris lineage that occupies springs of the northern Chihuahuan Desert, which is emerging in contemporary times. We investigated species boundaries using a validation-based approach and examined genetic structure of the lineage using a suite of microsatellite markers to identify independently evolving metapopulations. Our results show that each spring contains a genetically distinct population that is geographically isolated from other springs, suggesting evolutionary independence and status as separate species. Additionally, we observed subtle interspecific morphological variation among the putative species. We used multiple lines of evidence to formally describe four new species (Gammarus langi sp. nov., G. percalacustris sp. nov., G. colei sp. nov. and G. malpaisensis sp. nov.) endemic to the northern Chihuahuan Desert. Cryptic speciation is likely to be high in other aquatic taxa within these ecosystems, and across arid landscapes throughout North America and elsewhere, suggesting that the magnitude of the Linnean shortfall is currently underestimated in desert springs worldwide.

Past climate cooling promoted global dispersal of amphipods from Tian Shan montane lakes to circumboreal lakes

“…When G. lacustris spread across Eurasia, a lineage migrated from Tian Shan across Far East Asia and Beringia to North America (Brigham‐Grette, 2001). The development of lacustrine basins in the Rocky Mountain region triggered subsequent population isolation as a result of habitat insularity and poor dispersal potential (Adams et al, 2018; Walters et al, 2021).…”

“…We built ecological niche models (ENMs) to infer the possible distribution of G. lacustris in different climatic periods. A total of 3180 occurrence records (Data S2) were collected from the Global Biodiversity Information Facility (GBIF, http://gbif.org/), museums (Finland, https://laji.fi/en/observation/map?target=MX.214471%26sourceId=KE.3,KE.167; Norway, https://artsdatabanken.no/Taxon/Gammarus%2520lacustris/1919), literature (Adams et al, 2018; Clewing et al, 2016; Vainio & Vӓinӧlӓ, 2003; Walters et al, 2021) and our field work (Data S2). The data points cover most of the range of G. lacustris , except for the northern parts of Siberia; the absence of records in this region is due to lack of sampling and faunistic publications.…”

“…Therefore, G. lacustris can be used as a model system for understanding the global dispersal dynamics of montane‐lake organisms. Previous studies revealed that the regression of the Paratethys Sea promoted Gammarus colonization of freshwater habitats along the Tian Shan mountains (Hou et al, 2011), from which G. lacustris passed to montane lakes of the Alps (Alther et al, 2017; Vainio & Vӓinӧlӓ, 2003), Tibet (Clewing et al, 2016), and the Rocky Mountains (Adams et al, 2018; Walters et al, 2021).…”

Species boundaries to the limit: validating species delimitation methods is critical to avoid taxonomic inflation in the genomic era

“…Some of the mechanisms that can lead to a lack of phenotypical variation between divergent lineages include early divergence or niche conservatism (Fišer et al, 2018), among others. Moreover, the description of cryptic diversity is shortening the Linnean shortfall and is of paramount importance for conservation efforts (Walters, Cannizzaro, Trujillo, & Berg, 2021), since many species that were once thought to be homogeneous and widely distributed, actually represent complexes of cryptic species with sometimes endangered micro-endemic entities (Garcia-Porta, Simó-Riudalbas, Robinson, & Carranza, 2017). However, the lack of a specific threshold to distinguish separate evolutionary lineages from populations of the same species raises another challenging question: where do we stop?…”

Elevated salinity and temperature associated with climate change threaten the survival and conservation of desert spring amphipods

“…data). Gammarus in this region is composed of multiple species, each of which is restricted to a single spring system (Seidel, Lang & Berg, 2010; Adams et al, 2018; Walters et al, 2021). Three Chihuahuan Desert Gammarus species are federally listed as endangered, primarily as a result of threats to their habitat (USFWS, 2018).…”