Joint Effects of Inbreeding and Local Adaptation on the Evolution of Genetic Load after Fragmentation

Abstract: Disruption of gene flow among demes after landscape fragmentation can facilitate local adaptation but increase the effect of genetic drift and inbreeding. The joint effects of these conflicting forces on the mean fitness of individuals in a population are unknown. Through simulations, we explored the effect of increased isolation on the evolution of genetic load over the short and long term when fitness depends in part on local adaptation. We ignored genetic effects on demography. We modeled complex genomes, where a subset of the loci were under divergent selection in different localities. When a fraction of the loci were under heterogeneous selection, isolation increased mean fitness in larger demes made up of hundreds of individuals because of improved local adaptation. In smaller demes of tens of individuals, increased isolation improved local adaptation very little and reduced overall fitness. Short‐term improvement of mean fitness after fragmentation may not be indicative of the long‐term evolution of fitness. Whatever the deme size and potential for local adaptation, migration of one or two individuals per generation minimized the genetic load in general. The slow dynamics of mean fitness following fragmentation suggests that conservation measures should be implemented before the consequences of isolation on the genetic load become of concern.     

Long‐Term Impacts of Poaching on Relatedness,Stress Physiology,and Reproductive Output of Adult Female African Elephants

Abstract: Widespread poaching prior to the 1989 ivory ban greatly altered the demographic structure of matrilineal African elephant (Loxodonta africana) family groups in many populations by decreasing the number of old, adult females. We assessed the long‐term impacts of poaching by investigating genetic, physiological, and reproductive correlates of a disturbed social structure resulting from heavy poaching of an African elephant population in Mikumi National Park, Tanzania, prior to 1989. We examined fecal glucocorticoid levels and reproductive output among 218 adult female elephants from 109 groups differing in size, age structure, and average genetic relatedness over 25 months from 2003 to 2005. The distribution in group size has changed little since 1989, but the number of families with tusked old matriarchs has increased by 14.2%. Females from groups that lacked an old matriarch, first‐order adult relatives, and strong social bonds had significantly higher fecal glucocorticoid values than those from groups with these features (all females R²= 0.31; females in multiadult groups R²= 0.46). Females that frequented isolated areas with historically high poaching risk had higher fecal glucocorticoid values than those in low poaching risk areas. Females with weak bonds and low group relatedness had significantly lower reproductive output (R²[U]=0.21). Females from disrupted groups, defined as having observed average group relatedness 1 SD below the expected mean for a simulated unpoached family, had significantly lower reproductive output than females from intact groups, despite many being in their reproductive prime. These results suggest that long‐term negative impacts from poaching of old, related matriarchs have persisted among adult female elephants 1.5 decades after the 1989 ivory ban was implemented.     

Conservation Planning with Multiple Organizations and Objectives

Abstract: There has been a dramatic increase in the number of conservation organizations worldwide. It is now common for multiple organizations to operate in the same landscape in pursuit of different conservation goals. New objectives, such as maintenance of ecosystem services, will attract additional funding and new organizations to conservation. Systematic conservation planning helps in the design of spatially explicit management actions that optimally conserve multiple landscape features (e.g., species, ecosystems, or ecosystem services). But the methods used in its application implicitly assume that a single actor implements the optimal plan. We investigated how organizational behavior and conservation outcomes are affected by the presence of autonomous implementing organizations with different objectives. We used simulation models and game theory to explore how alternative behaviors (e.g., organizations acting independently or explicitly cooperating) affected an organization's ability to protect their feature of interest, and investigated how the distribution of features in the landscape influenced organizations’ attitudes toward cooperation. Features with highly correlated spatial distributions, although typically considered an opportunity for mutually beneficial conservation planning, can lead to organizational interactions that result in lower levels of protection. These detrimental outcomes can be avoided by organizations that cooperate when acquiring land. Nevertheless, for cooperative purchases to benefit both organizations’ objectives, each must forgo the protection of land parcels that they would consider to be of high conservation value. Transaction costs incurred during cooperation and the sources of conservation funding could facilitate or hinder cooperative behavior.     

Evaluating approaches for scaling-up community-based marine-protected areas into socially equitable and ecologically representative networks

Marine-protected areas (MPAs) are vital to marine conservation, but their coverage and distribution is insufficient to address declines in global biodiversity and fisheries. In response, many countries have committed through the Aichi Target 11 of the Convention on Biological Diversity to conserve 10% of the marine environment through ecologically representative and equitably managed MPAs by 2020. The rush to fulfill this commitment has raised concerns on how increasing MPA coverage will affect other elements of Target 11, including representation and equity. We examined a Philippines case study to assess and compare 3 MPA planning approaches for biodiversity representation and equitable distribution of costs to small-scale fishers. In the opportunistic approach, MPAs were identified and supported by coastal communities. The donor-assisted approach used local knowledge to select MPAs through a national-scale and donor-assisted conservation project. The systematic conservation planning approach identified MPA locations with the spatial prioritization software Marxan with Zones to achieve biodiversity objectives with minimal costs to fishers. We collected spatial data on biodiversity and fisheries features and performed a gap analysis to evaluate MPAs derived from different approaches. We assessed representation based on the proportion of biodiversity features conserved in MPAs and distribution equity by the distribution of opportunity costs (fishing areas lost in MPAs) among fisher stakeholder groups. The opportunistic approach did not ineffectively represent biodiversity and resulted in inequitable costs to fishers. The donor-assisted approach affected fishers disproportionately but provided near-optimal regional representation. Only the systematic approach achieved all representation targets with minimal and equitable costs to fishers. Our results demonstrate the utility of systematic conservation planning to address key elements of Target 11 and highlight opportunities (e.g., integration of local and scientific knowledge can address representation and equity concerns) and pitfalls (e.g., insufficient stakeholder considerations can exacerbate social inequalities) for planning MPAs in similar contexts.     

Incorporating differences between genetic diversity of trees and herbaceous plants in conservation strategies

Reviews that summarize the genetic diversity of plant species in relation to their life history and ecological traits show that forest trees have more genetic diversity at population and species levels than annuals or herbaceous perennials. In addition, among-population genetic differentiation is significantly lower in trees than in most herbaceous perennials and annuals. Possible reasons for these differences between trees and herbaceous perennials and annuals have not been discussed critically. Several traits, such as high rates of outcrossing, long-distance pollen and seed dispersal, large effective population sizes (N_e), arborescent stature, low population density, longevity, overlapping generations, and occurrence in late successional communities, may make trees less sensitive to genetic bottlenecks and more resistant to habitat fragmentation or climate change. We recommend that guidelines for genetic conservation strategies be designed differently for tree species versus other types of plant species. Because most tree species fit an LH scenario (low [L] genetic differentiation and high [H] genetic diversity), tree seeds could be sourced from a few populations distributed across the species’ range. For the in situ conservation of trees, translocation is a viable option to increase N_e. In contrast, rare herbaceous understory species are frequently HL (high differentiation and low diversity) species. Under the HL scenario, seeds should be taken from many populations with high genetic diversity. In situ conservation efforts for herbaceous plants should focus on protecting habitats because the typically small populations of these species are vulnerable to the loss of genetic diversity. The robust allozyme genetic diversity databases could be used to develop conservation strategies for species lacking genetic information. As a case study of reforestation with several tree species in denuded areas on the Korean Peninsula, we recommend the selection of local genotypes as suitable sources to prevent adverse effects and to insure the successful restoration in the long term.     

Reserve design to optimize functional connectivity and animal density

Ecological distance-based spatial capture–recapture models (SCR) are a promising approach for simultaneously estimating animal density and connectivity, both of which affect spatial population processes and ultimately species persistence. We explored how SCR models can be integrated into reserve-design frameworks that explicitly acknowledge both the spatial distribution of individuals and their space use resulting from landscape structure. We formulated the design of wildlife reserves as a budget-constrained optimization problem and conducted a simulation to explore 3 different SCR-informed optimization objectives that prioritized different conservation goals by maximizing the number of protected individuals, reserve connectivity, and density-weighted connectivity. We also studied the effect on our 3 objectives of enforcing that the space-use requirements of individuals be met by the reserve for individuals to be considered conserved (referred to as home-range constraints). Maximizing local population density resulted in fragmented reserves that would likely not aid long-term population persistence, and maximizing the connectivity objective yielded reserves that protected the fewest individuals. However, maximizing density-weighted connectivity or preemptively imposing home-range constraints on reserve design yielded reserves of largely spatially compact sets of parcels covering high-density areas in the landscape with high functional connectivity between them. Our results quantify the extent to which reserve design is constrained by individual home-range requirements and highlight that accounting for individual space use in the objective and constraints can help in the design of reserves that balance abundance and connectivity in a biologically relevant manner.     

The need for ecocentrism in biodiversity conservation

Over the past 5 decades, scientists have been documenting negative anthropogenic environmental change, expressing increasing alarm, and urging dramatic socioecological transformation in response. A host of international meetings have been held, but the erosion of biological diversity continues to accelerate. Why, then, has no effective political action been taken? We contend that part of the answer may lie in the anthropocentric ethical premises and moral rhetoric typically deployed in the cause of conservation. We further argue that it is essential to advance moral arguments for biodiversity conservation that are not just based on perceived human interests but on ecocentric values, namely, convictions that species and ecosystems have value and interests that should be respected regardless of whether they serve human needs and aspirations. A broader array of moral rationales for biodiversity conservation, we conclude, would be more likely to lead to effective plans, adopted and enforced by governments, designed to conserve biological diversity. A good place to start in this regard would be to explicitly incorporate ecocentric values into the recommendations that will be made at the conclusion of the 15th meeting of the parties to the Convention on Biological Diversity, scheduled to be held in October 2020.     

Overlooked biodiversity loss in tropical smallholder agriculture

Smallholder agriculture is the main driver of deforestation in the western Amazon, where terrestrial biodiversity reaches its global maximum. Understanding the biodiversity value of the resulting mosaics of cultivated and secondary forest is therefore crucial for conservation planning. However, Amazonian communities are organized across multiple forest types that support distinct species assemblages, and little is known about smallholder impacts across the range of forest types that are essential for sustaining biodiversity. We addressed this issue with a large-scale field inventory of birds (point counts) and trees (transects) in primary forest and smallholder agriculture in northern Peru across 3 forest types that are key for Amazonian biodiversity. For birds smallholder agriculture supported species richness comparable to primary forest within each forest type, but biotic homogenization across forest types resulted in substantial losses of biodiversity overall. These overall losses are invisible to studies that focus solely on upland (terra firma) forest. For trees biodiversity losses in upland forests dominated the signal across all habitats combined and homogenization across habitats did not exacerbate biodiversity loss. Proximity to forest strongly predicted the persistence of forest-associated bird and tree species in the smallholder mosaic, and because intact forest is ubiquitous in our study area, our results probably represent a best-case scenario for biodiversity in Amazonian agriculture. Land-use planning inside and outside protected areas should recognize that tropical smallholder agriculture has pervasive biodiversity impacts that are not apparent in typical studies that cover a single forest type. The full range of forest types must be surveyed to accurately assess biodiversity losses, and primary forests must be protected to prevent landscape-scale biodiversity loss.     

Incorporating connectivity into conservation planning for the optimal representation of multiple species and ecosystem services

Conservation planning tends to focus on protecting species’ ranges or landscape connectivity but seldom both—particularly in the case of diverse taxonomic assemblages and multiple planning goals. Therefore, information on potential trade-offs between maintaining landscape connectivity and achieving other conservation objectives is lacking. We developed an optimization approach to prioritize the maximal protection of species’ ranges, ecosystem types, and forest carbon stocks, while also including habitat connectivity for range-shifting species and dispersal corridors to link protected area. We applied our approach to Sabah, Malaysia, where the state government mandated an increase in protected-area coverage of approximately 305,000 ha but did not specify where new protected areas should be. Compared with a conservation planning approach that did not incorporate the 2 connectivity features, our approach increased the protection of dispersal corridors and elevational connectivity by 13% and 21%, respectively. Coverage of vertebrate and plant species’ ranges and forest types were the same whether connectivity was included or excluded. Our approach protected 2% less forest carbon and 3% less butterfly range than when connectivity features were not included. Hence, the inclusion of connectivity into conservation planning can generate large increases in the protection of landscape connectivity with minimal loss of representation of other conservation targets.     

Predicting the Probability of Outbreeding Depression

Abstract: Fragmentation of animal and plant populations typically leads to genetic erosion and increased probability of extirpation. Although these effects can usually be reversed by re‐establishing gene flow between population fragments, managers sometimes fail to do so due to fears of outbreeding depression (OD). Rapid development of OD is due primarily to adaptive differentiation from selection or fixation of chromosomal variants. Fixed chromosomal variants can be detected empirically. We used an extended form of the breeders’ equation to predict the probability of OD due to adaptive differentiation between recently isolated population fragments as a function of intensity of selection, genetic diversity, effective population sizes, and generations of isolation. Empirical data indicated that populations in similar environments had not developed OD even after thousands of generations of isolation. To predict the probability of OD, we developed a decision tree that was based on the four variables from the breeders’ equation, taxonomic status, and gene flow within the last 500 years. The predicted probability of OD in crosses between two populations is elevated when the populations have at least one of the following characteristics: are distinct species, have fixed chromosomal differences, exchanged no genes in the last 500 years, or inhabit different environments. Conversely, the predicted probability of OD in crosses between two populations of the same species is low for populations with the same karyotype, isolated for <500 years, and that occupy similar environments. In the former case, we recommend crossing be avoided or tried on a limited, experimental basis. In the latter case, crossing can be carried out with low probability of OD. We used crosses with known results to test the decision tree and found that it correctly identified cases where OD occurred. Current concerns about OD in recently fragmented populations are almost certainly excessive.