Has past climate change affected cold‐specialized species differentially through space and time?

Abstract

Quaternary climate change has been strongly linked to distributional shifts and recent species diversification. Montane species, in particular, have experienced enhanced isolation and rapid genetic divergence during glacial fluctuations, and these processes have resulted in a disproportionate number of neo-endemic species forming in high-elevation habitats. In temperate montane environments, a general model of alpine population history is well supported, where cold-specialized species track favourable climate conditions downslope during glacial episodes and upslope during warmer interglacial periods, which leads to a climate-driven population or species diversification pump. However, it remains unclear how geography mediates distributional changes and whether certain episodes of glacial history have differentially impacted rates of diversification. We address these questions by examining phylogenomic data in a North American clade of flightless, cold-specialized insects, the ice crawlers (Insecta: Grylloblattodea: Grylloblattidae: Grylloblatta). These low-vagility organisms have the potential to reveal highly localized refugia and patterns of spatial recolonization, as well as a longer history of in situ diversification. Using continuous phylogeographic analysis of species groups, we show that all species tend to retreat to nearby low-elevation habitats across western North America during episodes of glaciation, but species at high latitude exhibit larger distributional shifts. Lineage diversification was examined over the course of the Neogene and Quaternary periods, with statistical analysis supporting a direct association between climate variation and diversification rate. Major increases in lineage diversification appear to be correlated with warm and dry periods, rather than with extreme glacial events. Finally, we identify substantial cryptic diversity among ice crawlers, leading to high endemism across their range. This diversity provides new insights into highly localized glacial refugia for cold-specialized species across western North America.

Comparative transcriptomics of ice‐crawlers demonstrates cold specialization constrains niche evolution in a relict lineage

“…Further taxonomic sampling may improve estimates of these relationships. Finally, our results of relationships within Grylloblatta are consistent with a recent 322 gene nuclear phylogeny of 96 Grylloblatta samples (Schoville et al., 2019), with the exception that G . sp.…”

“…Grylloblatta samples (Schoville et al, 2019), with the exception that G. sp. "Sierra Buttes" is highly nested within California species in the transcriptome species tree (Figure 1).…”

Speciation of the cold‐adapted scorpionfly Cerapanorpa brevicornis (Mecoptera: Panorpidae) via interglacial refugia

“…The smaller population sizes in interglacial microrefugia might be strongly affected by the randomly accelerated genetic drift or local adaptation (Provan & Bennett, 2008; Stewart et al ., 2010; Camacho‐Sanchez et al ., 2018), thereby generating a deep genetic divergence from Lineage I. This situation also occurred in the Chinese mole shrew (He et al ., 2016), the summit rat (Camacho‐Sanchez et al ., 2018), the bumblebee (Martinet et al ., 2018), and the grylloblattids (Schoville et al ., 2019). The speciation event in C. brevicornis may provide further evidence to support the ‘Pleistocene species pump’ hypothesis, which states that Pleistocene interglacial warming can lead to speciation for cold‐adapted species between interglacial refugia after geographical isolation (Galbreath et al ., 2009; Martinet et al ., 2018).…”

“…Pleistocene climatic oscillations had profound impacts on the distributions of montane species globally (Avise, 2000; Hewitt, 2000, 2004). Periodical climatic cycles have driven species' ranges to shift repeatedly in both altitude and latitude, leading to alternating periods of isolation and connectivity (Hewitt, 2004; Stewart et al ., 2010; Schoville et al ., 2019). Periods of connectivity may allow for range expansions, dispersal, or gene flow, whereas periods of isolation may promote species genetic differentiation or even speciation (Carstens & Knowles, 2007; Waltari & Guralnick, 2009).…”

“…Climate‐driven genetic divergence or speciation events largely depend on local topography (Fjeldså et al ., 2012; Schoville et al ., 2019; Deng et al ., 2020). Topographically more diverse mountains generally harbour an exceptionally high biodiversity and endemicity (Fjeldså et al ., 2012; Rahbek et al ., 2019).…”