Using niche centrality within the scope of the nearly neutral theory of evolution to predict genetic diversity in a tropical conifer species‐pair

Abstract

Aim Estimating genetic diversity is key for understanging biogeographic and evolutionary processes. However, gathering genetic information is not feasible for all taxa or populations, particularly in the tropical regions. Identifying proxies for inferring such values has thus become essential. Here, we built on the niche centrality hypothesis (NCH; or central‐abundance hypothesis) and the nearly neutral theory of evolution (NNT) to identify some of such proxies using a montane tropical conifer species‐pair as model. The NCH predicts more genetic diversity under optimal ecological conditions, which should also allow for more efficient purifying selection, according to the NNT. Location The Transmexican Volcanic Belt, central Mexico. Taxa A fir species‐pair endemic to central Mexico, Abies flinckii and A.religiosa. Methods We estimated patterns of genetic diversity from nuclear SSRs (A, HE), and gene‐coding sequences (πS, πN), together with the efficacy of purifying selection, measured as πN/πS. After testing for niche overlap, we used several geographic and ecological proxies (i.e. longitude, latitude, elevation, estimated area and distance to the niche centroid in the present and in the LGM) to predict genetic diversity and πN/πS using general linear models. Results Populations at the west of the Trans Mexican Volcanic Belt (TVB) had lower genetic diversity than populations in the east of this mountain chain. Both species had significant niche overlap. The principal predictors for neutral genetic diversity (HE, A and πS) were longitude and latitude, followed by the current distance to the niche centroid; the efficiency of purifying selection was mostly accounted for by the current distance to the niche centroid (which was also correlated with elevation). No correlation was observed between genetic diversity or πN/πS and current population area. Main conclusions Historical and ecological factors have to be taken into account for explaining the amounts of genetic diversity in mountain tropical species. Following the NTT, populations closer to the niche centroid are more efficient at eliminating slightly deleterious mutations than marginal stands, independently of their size or geographic location (longitude). Expanding the central‐abundance theory within the scope of the NTT might help reconciling conflicting views concerning the extent of its empirical support.

Demographic modelling helps track the rapid and recent divergence of a conifer species pair from Central Mexico

“…It is not possible to estimate the cost of hybridization with the available data for these Mexican firs, which would require controlled cross‐pollination experiments and coding genomic information, but we could speculate on possible hypotheses to test in future studies. For instance, our results (Table 2, Figure 5a), and those of previous theoretical and empirical studies in these and other taxa, suggest that contrasting amounts of genetic load should be expected between species (Chen et al, 2017; Cruz‐Nicolás, Giles‐Pérez, Lira‐Noriega, et al, 2020; Ohta, 1992). Such a load would be more easily exposed in recombinant hybrids (i.e., F 2 , F 3 , … F n ) and backcrosses involving the parental species with the smallest N e (i.e., A. flinckii ) than in the opposite direction, which may result in reduced hybrid fitness (i.e., “hybrid load”; Moran et al, 2020; e.g., Christe et al, 2017; Fenster & Galloway, 2000; Hamilton et al, 2013; Moran et al, 2018), and explain the observed asymmetrical introgression from A. flinckii into A. religiosa (see also Pickup et al, 2019).…”

“…Such a contrasting distribution of inbreeding coefficients between western and eastern/central taxa remained unchanged when using data sets with other missing data thresholds (Material S2 ) and/or statistical approaches (Table S5 ), including popkin version 1.2.2, a method reputed to better reflect actual inbreeding than other method‐of‐moments estimators (Ochoa & Storey, 2021 ). However, even if the strict filters used herein did bias inbreeding estimates upwards (Material S2 ), high inbreeding and reduced genetic diversity are not new for western firs; they have been previously reported based on resequenced nuclear genes and simple sequence repteats (Cruz‐Nicolás, Giles‐Pérez, González‐Linares, et al, 2020 ; Cruz‐Nicolás, Giles‐Pérez, Lira‐Noriega, et al, 2020 ), plastid markers (Jaramillo‐Correa et al, 2008 ) and even allozymes (Aguirre‐Planter et al, 2000 ). These values point to an eventual transition from outcrossing to selfing in western firs, a mechanism recurrently reported in small conifer populations (Ledig et al, 1997 ; Robledo‐Arnuncio et al, 2004 ), and often invoked as a driver of speciation in plants (Cutter, 2019 ; Hopkins, 2013 ; Wright et al, 2013 ).…”

Complex genetic patterns and distribution limits mediated by native congeners of the worldwide invasive red‐eared slider turtle

“…To complement our findings regarding the niche centrality hypothesis, future comparisons between relative niche‐centre distances and genetic features (genetic diversity and genetic differentiation within and between species) could potentially improve predictions about sites with higher establishment risk. First to corroborate whether populations closer to the niche centre have higher abundance and are more genetically diverse (Cruz‐Nicolás et al, 2020), and second to elucidate the relationship between genetic distances and niche separation between closely related species (Tromas et al, 2018). Finally, our results set the basis for future work, where using whole genome or gene‐targeted sequencing and with the inclusion of a higher number of field‐sampled individuals would allow directly assessment of hybridization and specific gene introgression and connection between loci and traits.…”

“…To complement our findings regarding the niche centrality hypothesis, future comparisons between relative niche-centre distances and genetic features (genetic diversity and genetic differentiation within and between species) could potentially improve predictions about sites with higher establishment risk. First to corroborate whether populations closer to the niche centre have higher abundance and are more genetically diverse(Cruz-Nicolás et al, 2020), and second to elucidate the relationship between genetic distances and…”

Rules of Plant Species Ranges: Applications for Conservation Strategies

“…There are many examples where range position, niche position, and abundance do not correlate (Sagarin and Gaines, 2002;Eckert et al, 2008;Sexton et al, 2009Dallas et al, 2017;Pironon et al, 2017;Kennedy et al, 2020), and in some cases, plant population density actually increases towards range limits (e.g., . A growing body of research suggests that the history of a population is more indicative of its patterns of abundance and genetic variation than contemporary measures of the population's size, its range position, or the species' range size (Abeli et al, 2014;Koski et al, 2019;Cruz-Nicolás et al, 2020).…”