Evolutionary divergence in freshwater insects with contrasting dispersal capacity across a sea of desert

Abstract

Summary Arid landscapes pose arguably one of the greatest challenges to dispersal of aquatic insects, and may drive speciation in taxa with low dispersal potential. We investigated genetic divergence in aquatic insects with high and low dispersal potential between two regions within the Australian arid zone. We used two dragonfly species to infer patterns for strong‐dispersing species, and mayfly species from two genera to represent weak‐dispersing species. Based on dispersal‐related traits of the taxa, we predicted that dragonflies would show little divergence between and within the two geographical regions, while mayflies would show evidence of genetic isolation, with divergence timing associated with aridification in Australia. Samples were collected from perennial pools in ephemeral stream networks in central and western Australia. The two study regions are separated by approximately 1,500 km of predominantly dune desert. Collected insects were sequenced for one mitochondrial and one nuclear marker. We investigated spatial distribution of haplotypes, estimated divergence dates for identified mayfly lineages, and performed phylogenetic reconstruction to investigate relationships with known congeners. Both dragonfly species showed evidence of recent or ongoing gene flow between the central and western Australian study regions. In contrast, mayflies showed evidence of ancient, but not recent, gene flow between regions, with species‐level CO1 divergence within regions. We found 11 previously unknown putative mayfly species, that if confirmed could double the known diversity within these genera in Australia. Timing of divergence events for mayflies coincided with the development of the Australian arid zone, and phylogenetic relationships are similar to divergence patterns found in other Australian arid taxa. The findings of this study suggest that aridification is more likely to be a driver of diversification in taxa with low dispersal potential than in those with high dispersal potential. This is because effective aerial dispersal is integral for maintaining gene flow when aquatic connections are lost between distant populations, and reduced gene flow can promote genetic divergence.

Riverscape genetic variation, migration patterns, and morphological variation of the threatened Round Rocksnail, Leptoxis ampla

“…However, these fluvial characteristics have unequal influence on different organismal groups. For example, overland dispersal facilitates population connectivity of many aquatic insect groups (Geismar, Haase, Nowak, Sauer, & Pauls, ; Razeng et al, ), whereas such connectivity is improbable for fish and other species permanently bound to flowing rivers. Indeed, much of our understanding of gene flow and population genetic patterns in fluvial systems comes from studies of fish and aquatic insects (e.g.…”

“…Fluker et al, 2014a;Fluker, Kuhajda, & Harris, 2014b;Fluker et al, 2010;Prunier, Dubut, Loot, Tudesque, & Blanchet, 2017;Thomaz, Malabarba, & Knowles, 2017;Van Leeuwen, Dalen, Museth, Junge, & Vøllestad, 2018) and insects (e.g. Finn & Adler, 2006;Finn et al, 2007;Geismar et al, 2015;Múrria et al, 2017;Razeng et al, 2017). Of the few molecular studies that have employed population-level sampling of pleurocerids, none have revealed fine-scale landscape genetic patterns.…”

To remain or leave: Dispersal variation and its genetic consequences in benthic freshwater invertebrates

“…For example, studies on species of mayfly (with winged dispersal stage) and amphipods (dispersal via movement within streams) have revealed greater intrapopulation and overall genetic diversity for mayflies inhabiting streams and reservoirs relative to amphipods (Zickovich & Bohonak, 2007) and decreasing genetic diversity along upstream gradients for populations of an amphipod but not for those of a mayfly (Alp, Keller, Westram, & Robinson, 2012). Comparative analyses of dragonfly and mayfly species with relatively high and low dispersal potentials across groundwater-fed riverine pool systems in arid environments provided evidence for ongoing gene flow among dragonfly populations and substantial genetic divergence among mayfly populations (Razeng et al, 2017). Finally, populations of mussel species in smaller rivers were characterized by reduced genetic diversity relative to populations of other mussel species in larger rivers-a pattern linked with the relative movements of mussel larvae (glochidia) provided by smaller and larger fish species according to river size (Berg, Christian, & Guttman, 2007).…”

Redescription of Austrosimulium bancrofti (Taylor) (Diptera: Simuliidae): Australia’s second-worst problem black fly

“…) commented that A. bancrofti, unlike A. pestilens, occurred in dryer western Queensland and he wondered how populations survived-either with a drought resistant stage such as is known for A. pestilens, or by reintroduction when conditions were suitable. The latter point is of general interest to biogeographers of Australian arid regions (Razeng, et al, 2017;Majer et al, 2018). Indeed, Simulium ornatipes Skuse is known from southwest of Alice Springs at the George Gill Range, Northern Territories (S24.2556° E131.5702°), one of the driest regions in Australia (Davis et al,1993).…”