skip to main content


Title: Hybridization and endangered species protection in the molecular era
Abstract

After decades of discussion, there is little consensus on the extent to which hybrids between endangered and nonendangered species should be protected byUSlaw. As increasingly larger, genome‐scale data sets are developed, we can identify individuals and populations with even trace levels of genetic admixture, making the ‘hybrid problem’ all the more difficult. We developed a decision‐tree framework for evaluating hybrid protection, including both the processes that produced hybrids (human‐mediated or natural) and the ecological impact of hybrids on natural ecosystems. We then evaluated our decision tree for four case studies drawn from our own work and briefly discuss several other cases from the literature. Throughout, we highlight the management outcomes that our approach provides and the nuances of hybridization as a conservation problem.

 
more » « less
NSF-PAR ID:
10246026
Author(s) / Creator(s):
 ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Molecular Ecology
Volume:
25
Issue:
11
ISSN:
0962-1083
Page Range / eLocation ID:
p. 2680-2689
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Steep genetic clines resulting from recent secondary contact between previously isolated taxa can either gradually erode over time or be stabilized by factors such as ecological selection or selection against hybrids. We used patterns of variation in 30 nuclear and two mitochondrialSNPs to examine the factors that could be involved in stabilizing clines across a hybrid zone between two subspecies of the Atlantic killifish,Fundulus heteroclitus. Increased heterozygote deficit and cytonuclear disequilibrium in populations near the center of the mtDNAcline suggest that some form of reproductive isolation such as assortative mating or selection against hybrids may be acting in this hybrid zone. However, only a small number of loci exhibited these signatures, suggesting locus‐specific, rather than genomewide, factors. Fourteen of the 32 loci surveyed had cline widths inconsistent with neutral expectations, with twoSNPs in the mitochondrial genome exhibiting the steepest clines. Seven of the 12 putatively non‐neutral nuclear clines were forSNPs in genes related to oxidative metabolism. Among these putatively non‐neutral nuclear clines,SNPs in two nuclear‐encoded mitochondrial genes (SLC25A3 andHDDC2), as well asSNPs in the myoglobin, 40S ribosomal protein S17, and actin‐bindingLIMprotein genes, had clines that were coincident and concordant with the mitochondrial clines. When hybrid index was calculated using this subset of loci, the frequency distribution of hybrid indices for a population located at the mtDNAcline center was non‐unimodal, suggesting selection against advanced‐generation hybrids, possibly due to effects on processes involved in oxidative metabolism.

     
    more » « less
  2. Abstract Questions

    What are the primary biotic and abiotic factors driving composition and abundance of naturally regenerated tree seedlings across forest landscapes of Maine? Do seedling species richness (SR) and density (SD) decrease with improved growing conditions (climate and soil), but increase with increased diversity of overstorey composition and structure? Does partial harvesting disproportionately favour relative dominance of shade‐intolerant hardwoods (PIHD) over shade‐tolerant softwoods (PTSD)?

    Location

    Forest landscapes across the diverse eco‐regions and forest types of Maine,USA.

    Methods

    This study usedUSDAForest Service Forest Inventory Analysis permanent plots (n = 10 842), measured every 5 yr since 1999. The best models for each response variable (SR,SD,PIHDandPTSD) were developed based onAICand biological interpretability, while considering 35 potential explanatory variables incorporating climate, soil, site productivity, overstorey structure and composition, and past harvesting.

    Results

    Mean annual temperature was the most important abiotic factor, whereas overstorey tree size diversity was the most important biotic factor forSRandSD. Both mean annual temperature and overstorey tree size diversity had a curvilinear relationship withSRandSD. Average overstorey shade tolerance and percentage tolerant softwood basal area in the overstorey were the top predictor variables ofPIHDandPTSD,respectively. Partial harvesting favouredPIHDbut notPTSD.

    Conclusions

    This is one of the first studies to comprehensively evaluate a number of factors influencing naturally established tree seedlings at a broad landscape scale in the Northern Forest region of the easternUSAand Canada. Despite limitations associated with relatively small plot size, large seedling size class and lack of direct measurements of light, water and nutrients, this study documents the influence of these factors amid high variability associated with patterns of natural regeneration. The curvilinear relationship between mean annual temperature withSRandSDsupports the argument that species richness and abundance usually have unimodal relationships with productivity indicators, whereas the curvilinear relationship between overstorey tree size diversity andSRandSDsuggest that moderate overstorey diversity incorporates multiple species as well as higher seedling individuals.

     
    more » « less
  3. Abstract

    The arrival to theUnitedStates of theAfricanized honey bee, a hybrid betweenEuropean subspecies and theAfrican subspeciesApis mellifera scutellata, is a remarkable model for the study of biological invasions. This immigration has created an opportunity to study the dynamics of secondary contact of honey bee subspecies fromAfrican andEuropean lineages in a feral population inSouthTexas. An 11‐year survey of this population (1991–2001) showed that mitochondrial haplotype frequencies changed drastically over time from a resident population of eastern and western European maternal ancestry, to a population dominated by theAfrican haplotype. A subsequent study of the nuclear genome showed that theAfricanization process included bidirectional gene flow between European and Africanized honey bees, giving rise to a new panmictic mixture ofA. m. scutellata‐and European‐derived genes. In this study, we examined gene flow patterns in the same population 23 years after the first hybridization event occurred. We found 28 active colonies inhabiting 92 tree cavities surveyed in a 5.14 km2area, resulting in a colony density of 5.4 colonies/km2. Of these 28 colonies, 25 were ofA. m. scutellatamaternal ancestry, and three were of western European maternal ancestry. No colonies of eastern European maternal ancestry were detected, although they were present in the earlier samples. NuclearDNArevealed little change in the introgression ofA. m. scutellata‐derived genes into the population compared to previous surveys. Our results suggest this feral population remains an admixed swarm with continued low levels of European ancestry and a greater presence of African‐derived mitochondrial genetic composition.

     
    more » « less
  4. Abstract

    Whether niche processes, like environmental filtering, or neutral processes, like dispersal limitation, are the primary forces driving community assembly is a central question in ecology. Here, we use a natural experimental system of isolated tree “islands” to test whether environment or geography primarily structures fungal community composition at fine spatial scales. This system consists of isolated pairs of two distantly related, congeneric pine trees established at varying distances from each other and the forest edge, allowing us to disentangle the effects of geographic distance vs. host and edaphic environment on associated fungal communities. We identified fungal community composition with Illumina sequencing ofITSamplicons, measured all relevant environmental parameters for each tree—including tree age, size and soil chemistry—and calculated geographic distances from each tree to all others and to the nearest forest edge. We applied generalized dissimilarity modelling to test whether total and ectomycorrhizal fungal (EMF) communities were primarily structured by geographic or environmental filtering. Our results provide strong evidence that as in many other organisms, niche and neutral processes both contribute significantly to turnover in community composition in fungi, but environmental filtering plays the dominant role in structuring both free‐living and symbiotic fungal communities at fine spatial scales. In our study system, we foundpHand organic matter primarily drive environmental filtering in total soil fungal communities and thatpHand cation exchange capacity—and, surprisingly, not host species—were the largest factors affectingEMFcommunity composition. These findings support an emerging paradigm thatpHmay play a central role in the assembly of all soil‐mediated systems.

     
    more » « less
  5. Abstract

    Heterospecific mating frequency is critical to hybrid zone dynamics and can directly impact the strength of reproductive barriers and patterns of introgression. The effectiveness of post‐mating prezygotic (PMPZ) reproductive barriers, which include reduced fecundity via heterospecific matings and conspecific sperm precedence, may depend on the number, identity and order of mates. Studies ofPMPZbarriers suggest that they may be important in many systems, but whether these barriers are effective at realistic heterospecific mating frequencies has not been tested. Here, we evaluate the strength of cryptic reproductive isolation in two leaf beetles (Chrysochus auratusandC. cobaltinus) in the context of a range of heterospecific mating frequencies observed in natural populations. We found both species benefited from multiple matings, but the benefits were greater inC. cobaltinusand extended to heterospecific matings. We found thatPMPZbarriers greatly limited hybrid production byC. auratusfemales with moderate heterospecific mating frequencies, but that their effectiveness diminished at higher heterospecific mating frequencies. In contrast, there was no evidence forPMPZbarriers inC. cobaltinusfemales at any heterospecific mating frequency. We show that integrating realistic estimates of cryptic isolation with information on relative abundance and heterospecific mating frequency in the field substantially improves our understanding of the strong directional bias in F1 production previously documented in theChrysochushybrid zone. Our results demonstrate that heterospecific mating frequency is critical to understanding the impact of cryptic post‐copulatory barriers on hybrid zone structure and dynamics, and that future studies of such barriers should incorporate field‐relevant heterospecific mating frequencies.

     
    more » « less