skip to main content


Title: Evolutionary stability, landscape heterogeneity, and human land‐usage shape population genetic connectivity in the Cape Floristic Region biodiversity hotspot
Abstract

As human‐induced change eliminates natural habitats, it impacts genetic diversity and population connectivity for local biodiversity. The South African Cape Floristic Region (CFR) is the most diverse extratropical area for plant biodiversity, and much of its habitat is protected as a UNESCO World Heritage site. There has long been great interest in explaining the underlying factors driving this unique diversity, especially as much of the CFR is endangered by urbanization and other anthropogenic activity. Here, we use a population and landscape genetic analysis of SNP data from the CFR endemic plantLeucadendron salignumor “common sunshine conebush” as a model to address the evolutionary and environmental factors shaping the vast CFR diversity. We found that high population structure, along with relatively deeper and older genealogies, is characteristic of the southwestern CFR, whereas low population structure and more recent lineage coalescence depict the eastern CFR. Population network analyses show genetic connectivity is facilitated in areas of lower elevation and higher seasonal precipitation. These population genetic signatures corroborate CFR species‐level patterns consistent with high Pleistocene biome stability and landscape heterogeneity in the southwest, but with coincident instability in the east. Finally, we also find evidence of human land‐usage as a significant gene flow barrier, especially in severely threatened lowlands where genetic connectivity has been historically the highest. These results help identify areas where conservation plans can prioritize protecting high genetic diversity threatened by contemporary human activities within this unique cultural UNESCO site.

 
more » « less
NSF-PAR ID:
10369333
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Evolutionary Applications
Volume:
14
Issue:
4
ISSN:
1752-4571
Format(s):
Medium: X Size: p. 1109-1123
Size(s):
["p. 1109-1123"]
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Apex predators are important indicators of intact natural ecosystems. They are also sensitive to urbanization because they require broad home ranges and extensive contiguous habitat to support their prey base. Pumas (Puma concolor) can persist near human developed areas, but urbanization may be detrimental to their movement ecology, population structure, and genetic diversity. To investigate potential effects of urbanization in population connectivity of pumas, we performed a landscape genomics study of 130 pumas on the rural Western Slope and more urbanized Front Range of Colorado, USA. Over 12,000 single nucleotide polymorphisms (SNPs) were genotyped using double‐digest, restriction site‐associated DNA sequencing (ddRADseq). We investigated patterns of gene flow and genetic diversity, and tested for correlations between key landscape variables and genetic distance to assess the effects of urbanization and other landscape factors on gene flow. Levels of genetic diversity were similar for the Western Slope and Front Range, but effective population sizes were smaller, genetic distances were higher, and there was more admixture in the more urbanized Front Range. Forest cover was strongly positively associated with puma gene flow on the Western Slope, while impervious surfaces restricted gene flow and more open, natural habitats enhanced gene flow on the Front Range. Landscape genomic analyses revealed differences in puma movement and gene flow patterns in rural versus urban settings. Our results highlight the utility of dense, genome‐scale markers to document subtle impacts of urbanization on a wide‐ranging carnivore living near a large urban center.

     
    more » « less
  2. Abstract

    Urban fragmentation can reduce gene flow that isolates populations, reduces genetic diversity and increases population differentiation, all of which have negative conservation implications. Alternatively, gene flow may actually be increased among urban areas consistent with an urban facilitation model. In fact, urban adapter pests are able to thrive in the urban environment and may be experiencing human‐mediated transport. Here, we used social network theory with a population genetic approach to investigate the impact of urbanization on genetic connectivity in the Western black widow spider, as an urban pest model of human health concern. We collected genomewide single nucleotide polymorphism variation from mitochondrial and nuclear double‐digest RAD (ddRAD) sequence data sets from 210 individuals sampled from 11 urban and 10 nonurban locales across its distribution of the Western United States. From urban and nonurban contrasts of population, phylogenetic, and network analyses, urban locales have higher within‐population genetic diversity, lower between‐population genetic differentiation and higher estimates of genetic connectivity. Social network analyses show that urban locales not only have more connections, but can act as hubs that drive connectivity among nonurban locales, which show signatures of historical isolation. These results are consistent with an urban facilitation model of gene flow and demonstrate the importance of sampling multiple cities and markers to identify the role that urbanization has had on larger spatial scales. As the urban landscape continues to grow, this approach will help determine what factors influence the spread and adaptation of pests, like the venomous black widow spider, in building policies for human and biodiversity health.

     
    more » « less
  3. BACKGROUND The Republic of Madagascar is home to a unique assemblage of taxa and a diverse set of ecosystems. These high levels of diversity have arisen over millions of years through complex processes of speciation and extinction. Understanding this extraordinary diversity is crucial for highlighting its global importance and guiding urgent conservation efforts. However, despite the detailed knowledge that exists on some taxonomic groups, there are large knowledge gaps that remain to be filled. ADVANCES Our comprehensive analysis of major taxonomic groups in Madagascar summarizes information on the origin and evolution of terrestrial and freshwater biota, current species richness and endemism, and the utilization of this biodiversity by humans. The depth and breadth of Madagascar’s biodiversity—the product of millions of years of evolution in relative isolation —is still being uncovered. We report a recent acceleration in the scientific description of species but many remain relatively unknown, particularly fungi and most invertebrates. DIGITIZATION Digitization efforts are already increasing the resolution of species richness patterns and we highlight the crucial role of field- and collections-based research for advancing biodiversity knowledge in Madagascar. Phylogenetic diversity patterns mirror that of species richness and endemism in most of the analyzed groups. Among the new data presented, our update on plant numbers estimates 11,516 described vascular plant species native to Madagascar, of which 82% are endemic, in addition to 1215 bryophyte species, of which 28% are endemic. Humid forests are highlighted as centers of diversity because of their role as refugia and centers of recent and rapid radiations, but the distinct endemism of other areas such as the grassland-woodland mosaic of the Central Highlands and the spiny forest of the southwest is also important despite lower species richness. Endemism in Malagasy fungi remains poorly known given the lack of data on the total diversity and global distribution of species. However, our analysis has shown that ~75% of the fungal species detected by environmental sequencing have not been reported as occurring outside of Madagascar. Among the 1314 species of native terrestrial and freshwater vertebrates, levels of endemism are extremely high (90% overall)—all native nonflying terrestrial mammals and native amphibians are found nowhere else on Earth; further, 56% of the island’s birds, 81% of freshwater fishes, 95% of mammals, and 98% of reptile species are endemic. Little is known about endemism in insects, but data from the few well-studied groups on the island suggest that it is similarly high. The uses of Malagasy species are many, with much potential for the uncovering of useful traits for food, medicine, and climate mitigation. OUTLOOK Considerable work remains to be done to fully characterize Madagascar’s biodiversity and evolutionary history. The multitudes of known and potential uses of Malagasy species reported here, in conjunction with the inherent value of this unique and biodiverse region, reinforce the importance of conserving this unique biota in the face of major threats such as habitat loss and overexploitation. The gathering and analysis of data on Madagascar’s remarkable biota must continue and accelerate if we are to safeguard this unique and highly threatened subset of Earth’s biodiversity. Emergence and composition of Madagascar’s extraordinary biodiversity. Madagascar’s biota is the result of over 160 million years of evolution, mostly in geographic isolation, combined with sporadic long distance immigration events and local extinctions. (Left) We show the age of the oldest endemic Malagasy clade for major groups (from bottom to top): arthropods, bony fishes, reptiles, flatworms, birds, amphibians, flowering plants, mammals, non-flowering vascular plants, and mollusks). Humans arrived recently, some 10,000 to 2000 years (top right) and have directly or indirectly caused multiple extinctions (including hippopotamus, elephant birds, giant tortoises, and giant lemurs) and introduced many new species (such as dogs, zebu, rats, African bushpigs, goats, sheep, rice). Endemism is extremely high and unevenly distributed across the island (the heat map depicts Malagasy palm diversity, a group characteristic of the diverse humid forest). Human use of biodiversity is widespread, including 1916 plant species with reported uses. The scientific description of Malagasy biodiversity has accelerated greatly in recent years (bottom right), yet the diversity and evolution of many groups remain practically unknown, and many discoveries await. 
    more » « less
  4. Abstract

    Natural landscape heterogeneity and barriers resulting from urbanization can reduce genetic connectivity between populations. The evolutionary, demographic, and ecological effects of reduced connectivity may lead to population isolation and ultimately extinction. Alteration to the terrestrial and aquatic environment caused by urban influence can affect gene flow, specifically for stream salamanders who depend on both landscapes for survival and reproduction. To examine how urbanization affects a relatively common stream salamander species, we compared genetic connectivity ofEurycea bislineata(northern two‐lined salamander) populations within and between streams in an urban, suburban, and rural habitat around the New York City (NYC) metropolitan area. We report reduced genetic connectivity between streams within the urban landscape found to correspond with potential barriers to gene flow, that is, areas with more dense urbanization (roadways, industrial buildings, and residential housing). The suburban populations also exhibited areas of reduced connectivity correlated with areas of greater human land use and greater connectivity within a preserve protected from development. Connectivity was relatively high among neighboring rural streams, but a major roadway corresponded with genetic breaks even though the habitat contained more connected green space overall. Despite greater human disturbance across the landscape, urban and suburban salamander populations maintained comparable levels of genetic diversity to their rural counterparts. Yet small effective population size in the urban habitats yielded a high probability of loss of heterozygosity due to genetic drift in the future. In conclusion, urbanization impacted connectivity among stream salamander populations where its continual influence may eventually hinder population persistence for this native species in urban habitats.

     
    more » « less
  5. Abstract

    Landscape heterogeneity can shape genetic structure and functional connectivity of populations. When this heterogeneity imposes variable costs of moving across the landscape, populations can be structured according to a pattern of “isolation by resistance” (IBR). At the same time, divergent local environmental filters can limit gene flow, creating an alternative pattern of “isolation by environment” (IBE). Here, we evaluate IBR and IBE in the insect‐pollinated, biennial plantSabatia angularis(L.) Pursh (Gentianaceae) across serpentine grasslands in the fragmented landscape of SE Pennsylvania, USA using ~4500 neutral SNP loci. Specifically, we test the extent to which radical alteration of the landscape matrix by humans has fundamentally altered the cost of movement, imprinting a pattern of IBR dictated by land use type and intensity, and the potential for IBE in relation to a gradient of heavy metal concentrations found in serpentine soil. We reveal a strong signal of IBR and a weak signal of IBE across sites, indicating the greater importance of the landscape matrix in shaping genetic structure ofS. angularispopulations in the study region. Based on Circuitscape and least cost path approaches, we find that both low‐ and high‐intensity urbanization resist gene flow by orders of magnitude greater than “natural” habitats, although resistance to low‐intensity urbanization weakens at larger spatial scales. While cropland presents a substantially lower barrier than urban development, cumulative human land use surrounding populations predicts within‐population genetic diversity and inbreeding inS. angularis. Our results emphasize the role of forest buffers and corridors in facilitating gene flow between serpentine grassland patches and averting local extinction of plant populations.

     
    more » « less