Postglacial migration across a large dispersal barrier outpaces regional expansion from glacial refugia: evidence from two conifers in the Pacific Northwest

Abstract

Understanding how climate refugia and migration over great distances have facilitated species survival during periods of past climate change is crucial for evaluating contemporary threats to biodiversity. In addition to tracking a changing climate, extant species must face complex, anthropogenically fragmented landscapes. The dominant conifer species in the mesic temperate forests of the Pacific Northwest are split by the arid rain-shadow of the Cascade Range into coastal and interior distributions, with continued debate over the origins of the interior populations. If the Last Glacial Maximum extirpated populations in the interior then postglacial migration across the arid divide would have been necessary to create the current distribution, whereas interior refugial persistence could have locally repopulated the disjunction. These alternative scenarios have significant implications for the postglacial development of the Pacific Northwest mesic forests and the impact of dispersal barriers during periods of climate change. Here we use genotyping-by-sequencing (ddRADseq) and phylogeographical modeling to show that the postglacial expansion of both mountain hemlock and western redcedar consisted largely of long-distance spread inland in the direction of dominant winds, with limited expansion from an interior redcedar refugium. Our results for these two key mesic conifers, along with fossil pollen data, address the longstanding question on the development of the Pacific Northwest mesic forests and contrast with many recent studies emphasizing the role of cryptic refugia in colonizing modern species ranges. Statement of SignificanceUnderstanding whether habitat fragmentation hinders range shifts as species track a changing climate presents a pressing challenge for biologists. Species with disjunct distributions provide a natural laboratory for studying the effects of fragmentation during past periods of climate change. We find that dispersal across a 50-200-km inhospitable barrier characterized the expansion of two conifer species since the last ice age. The importance of migration, and minimal contribution of more local glacial refugia, contrasts with many recent studies emphasizing the role of microrefugia in populating modern species distributions. Our results address a longstanding question on the development of the disjunct mesic conifer forests of the Pacific Northwest and offer new insights into the spatiotemporal patterns of refugial populations and postglacial vegetation development previously unresolved despite decades of paleoecological studies.

Ice‐age persistence and genetic isolation of the disjunct distribution of larch in Alaska

“…These analyses also revealed complex postglacial population dynamics, uncovering the interplay between refugial persistence and long-distance migration (Escudero, Valcárcel, Vargas, & Luceño, 2010;Fernandez, Hu, Gavin, de Lafontaine, & Heath, 2020;Wolf, Schneider, & Ranker, 2001). For example, although refugial populations of Thuja plicata persisted through the LGM in the interior of the Pacific Northwest, long-distance immigrants from coastal populations dominated the interior range expansion during the postglacial period (Fernandez et al, 2020). Tamarack (eastern larch, Larix laricina) is a transcontinental North American conifer, with a prominent disjunction in the Yukon that isolates the Alaskan distribution from the larger range in Canada (Ritchie, 1987;Warren et al, 2016).…”

“…Genetic analyses of disjunct populations from a number of species, such as Pinus nigra in western Europe, have highlighted the role of LGM refugia in postglacial colonization (e.g., Afzal‐Rafii & Dodd, ). These analyses also revealed complex postglacial population dynamics, uncovering the interplay between refugial persistence and long‐distance migration (Escudero, Valcárcel, Vargas, & Luceño, ; Fernandez, Hu, Gavin, de Lafontaine, & Heath, 2020; Wolf, Schneider, & Ranker, ). For example, although refugial populations of Thuja plicata persisted through the LGM in the interior of the Pacific Northwest, long‐distance immigrants from coastal populations dominated the interior range expansion during the postglacial period (Fernandez et al, 2020).…”

Evolutionary response of cold‐adapted chasmophytic plants to Quaternary climatic oscillations in the Mountains of Central Asia (a world hotspot of biodiversity)

“…There are two main demographic responses to climate changes of cold‐adapted species: (a) increase in population sizes during glaciations and a decrease in interglacials mainly due to temperature rise, the so‐called ‘interglacial refugia model’ (Bennett & Provan, 2008; He et al, 2015; Ortego et al, 2021; Ortego & Knowles, 2022; Tonzo & Ortego, 2021; Vintsek et al, 2022; Yang et al, 2022), and (b) decrease in population sizes during glaciations and an increase in population sizes during interglacials (expansion from glacial refugia). The second one is mainly due to the rise in temperature and subsequent increase of suitable habitat areas, typical for lower elevation species (Fernandez et al, 2020; Guerrina et al, 2022; Wielstra et al, 2013), and more exceptionally, for plants from high‐mountain plateaus (Muellner‐Riehl, 2019; Wróbel et al, 2023). Our results for the demographic population reconstruction are in line with the first mentioned above response and show that many of analysed populations of C. eugeniae and C. lehmanniana underwent parallel and substantial changes in effective population size with similar trajectories, and right after LGM, they experienced an extraordinary decline of effective population size.…”