Do different rates of gene flow underlie variation in phenotypic and phenological clines in a montane grasshopper community?

Abstract

Species responses to environmental change are likely to depend on existing genetic and phenotypic variation, as well as evolutionary potential. A key challenge is to determine whether gene flow might facilitate or impede genomic divergence among populations responding to environmental change, and if emergent phenotypic variation is dependent on gene flow rates. A general expectation is that patterns of genetic differentiation in a set of codistributed species reflect differences in dispersal ability. In less dispersive species, we predict greater genetic divergence and reduced gene flow. This could lead to covariation in life-history traits due to local adaptation, although plasticity or drift could mirror these patterns. We compare genome-wide patterns of genetic structure in four phenotypically variable grasshopper species along a steep elevation gradient near Boulder, Colorado, and test the hypothesis that genomic differentiation is greater in short-winged grasshopper species, and statistically associated with variation in growth, reproductive, and physiological traits along this gradient. In addition, we estimate rates of gene flow under competing demographic models, as well as potential gene flow through surveys of phenological overlap among populations within a species. All species exhibit genetic structure along the elevation gradient and limited gene flow. The most pronounced genetic divergence appears in short-winged (less dispersive) species, which also exhibit less phenological overlap among populations. A high-elevation population of the most widespread species, Melanoplus sanguinipes, appears to be a sink population derived from low elevation populations. While dispersal ability has a clear connection to the genetic structure in different species, genetic distance does not predict growth, reproductive, or physiological trait variation in any species, requiring further investigation to clearly link phenotypic divergence to local adaptation. K E Y W O R D S climate change, elevational gradient, gene flow, local adaptation, population genetics, Rocky Mountains | 981 SLATYER ET AL.

Phenology and plasticity can prevent adaptive clines in thermal tolerance across temperate mountains: The importance of the elevation‐time axis

“…The prevalence of intraspecific adaptive clinal variation with elevation in thermal traits is still a contentious topic in current literature. Although several studies have found support for this pattern in both Critical Thermal Limits (Bishop et al, 2017 ; Klok & Chown, 2003 ; Miller & Packard, 1977 ; Sørensen et al, 2005 ) with greater variation in CT min than CT max (Gilbert & Miles, 2019 ; Muñoz et al, 2014 ), many others did not (Buckley et al, 2013 ; Gvoždík & Castilla, 2001 ; Slatyer et al, 2016 ; Slatyer & Schoville, 2016 ; Senior et al, 2019 ; Slatyer et al, 2019 ; Tonione et al, 2020 ; Enriquez‐Urzelai et al, 2018 , 2020 ). The lack of clinal variation in R. parvipalmata contrasts with the observation of local adaptation in larval life history traits of other temperate amphibians in seasonal thermal gradients (Berven et al, 1979 ; Luquet et al, 2015 ; Richter‐Boix et al, 2015 ), including the closely related Rana temporaria (Laugen et al, 2003 ; Lind et al, 2011 ; Muir et al, 2014 ).…”

“…Recent intraspecific studies have revealed adaptive clinal variation with elevation in both CT max and CT min (Bishop et al, 2017;Klok & Chown, 2003;Sørensen et al, 2005) with more variation in CT min than CT max (Muñoz et al, 2014). In contrast, a number of studies did not reveal such elevational trend in physiological traits related to thermal tolerances (Buckley et al, 2013;Gvoždík & Castilla, 2001;Senior et al, 2019;Slatyer et al, 2019;Slatyer & Schoville, 2016;Tonione et al, 2020). Yet, reliable data to support adaptive clinal variation is still scant because of the need and difficulty of integrating phenotypic (P ST ) and molecular divergence (F ST ) (Brommer, 2011;Leinonen et al, 2008).…”

Grasshopper species' seasonal timing underlies shifts in phenological overlap in response to climate gradients, variability and change

“…We note that species in our analyses differ in dispersal ability (due to wing length differences) and lower rates of gene flow may result in a greater degree of local adaptation (Kawecki & Ebert, 2004;Slatyer et al, 2020;Wagner & Liebherr, 1992). Chloealtis abdominalis, M. dawsoni, M. boulderensis and A. clavatus have short wings and are least dispersive.…”

High-Elevation Populations of Montane Grasshoppers Exhibit Greater Developmental Plasticity in Response to Seasonal Cues

“…M. boulderensis grasshoppers can lay egg pods every few days and individuals can persist as adults for at least a month at 3,048 m site (Nufio unpublished data), so faster development may allow production of more egg pods. Higher-elevation populations of M. boulderensis exhibit smaller eggs and clutches ( Levy and Nufio, 2014 ; Slatyer et al, 2020 ), consistent with laying more clutches. Alternatively, observed developmental plasticity may enable rapid early-season development to avoid resource competition with other species when conditions are permissive.…”