Accumulation of Mutational Load at the Edges of a Species Range

Abstract

Why species have geographically restricted distributions is an unresolved question in ecology and evolutionary biology. Here, we test a new explanation that mutation accumulation due to small population size or a history of range expansion can contribute to restricting distributions by reducing population growth rate at the edge. We examined genomic diversity and mutational load across the entire geographic range of the North American plant Arabidopsis lyrata, including old, isolated populations predominantly at the southern edge and regions of postglacial range expansion at the northern and southern edges. Genomic diversity in intergenic regions declined toward distribution edges and signatures of mutational load in exon regions increased. Genomic signatures of mutational load were highly linked to phenotypically expressed load, measured as reduced performance of individual plants and lower estimated rate of population growth. The geographic pattern of load and the connection between load and population growth demonstrate that mutation accumulation reduces fitness at the edge and helps restrict species' distributions.

Genetic drift during the spread phase of a biological invasion

“…These variations in allelic frequencies possibly indicate recent and even ongoing bottlenecks, as evidenced by the loss of rare alleles observed between 2014 and 2016; however, in the case of a range expansion they could also reflect the long‐lasting effects of bottlenecks linked to the colonization process. The observed dynamics of genetic diversity potentially bears important ecological and evolutionary consequences for populations located at the edges of the invasion, such as decreases in individual fitness and in population growth rates (Peischl et al, ; Willi et al, ).…”

Eco‐evolution on the edge during climate change

“…First, repeated founder events and genetic drift in small, newly established populations on the range front can reduce genetic variation (Phillips 2012, Polechova 2018). Many species have reduced genetic variation on their cool range margin due to past range expansions (Hewitt 2000, González-Martínez et al 2017, Pironon et al 2017, Willi et al 2018, and experiments demonstrate that this low genetic variation can limit responses to selection in newly colonized locations (Pujol and Pannell 2008). Also, simulations suggest range-front populations are less likely to adapt to novel conditions encountered later in the range-expansion process when genetic variation is lower (Phillips 2012).…”

“…Once established on the range front, deleterious alleles can move with the expanding front in a process known as gene surfing (Excoffier et al 2009). Moreover, deleterious mutations often persist on range margins during experimental range expansions (Bosshard et al 2017, Weiss-Lehman et al 2017) and on cool range margins after historical range expansions in nature (González-Martínez et al 2017, Willi et al 2018. Several models have demonstrated deleterious gene surfing and its effects on range expansion (Peischl and Excoffier 2015, Gilbert et al 2017.…”

Postglacial ecotype formation under outcrossing and self‐fertilization inArabidopsis lyrata

“…Even though adaptation to substrate might have occurred before the shift to selfing in many areas of the current range of A. lyrata , the phenotypic results indicates that the maintenance of trait divergence by directional selection has not been constrained by genetic drift. We conclude that directional selection must have been strong, because for the same populations studied, good evidence for decreased efficacy of purifying selection had been found previously selfing and long‐term small outcrossing populations ere shown to have accumulated mutational load that translated into reduced population performance under common garden conditions (Willi Evolution; Willi et al Heredity; Willi et al, ). Selfing does not seem to preclude the maintenance of considerable adaptive divergence to environmental heterogeneity.…”

“…The species is a short‐lived perennial and hermaphroditic plant, and it is closely related to the model species A. thaliana (Hohmann et al, ). Following the retreat of the glaciers starting about ~20'000 years ago, A. lyrata underwent a range expansion in North America (Griffin & Willi, ; Willi, Fracassetti, Zoller, & Van Buskirk, ) and colonized distinct substrates that can be broadly categorized as rock and sand (Willi & Määttänen, ; Figure , Supporting Information Table ). Rocky substrates comprise, for example, bare mountaintops of the Appalachians, bare rocky shores of larger lakes and bare cliffs along rivers, while sandy sites include sand dunes on lakes, sand deposits along rivers and eroded sandstone.…”