Phenotypes in phylogeography Zamudio, Kelly R.; Bell, Rayna C.; Mason, Nicholas A.
Proceedings of the National Academy of Sciences - PNAS,
07/2016, Volume:
113, Issue:
29
Journal Article
Peer reviewed
Open access
Almost 30 y ago, the field of intraspecific phylogeography laid the foundation for spatially explicit and genealogically informed studies of population divergence. With new methods and markers, the ...focus in phylogeography shifted to previously unrecognized geographic genetic variation, thus reducing the attention paid to phenotypic variation in those same diverging lineages. Although phenotypic differences among lineages once provided the main data for studies of evolutionary change, the mechanisms shaping phenotypic differentiation and their integration with intraspecific genetic structure have been underexplored in phylogeographic studies. However, phenotypes are targets of selection and play important roles in species performance, recognition, and diversification. Here, we focus on three questions. First, how can phenotypes elucidate mechanisms underlying concordant or idiosyncratic responses of vertebrate species evolving in shared landscapes? Second, what mechanisms underlie the concordance or discordance of phenotypic and phylogeographic differentiation? Third, how can phylogeography contribute to our understanding of functional phenotypic evolution? We demonstrate that the integration of phenotypic data extends the reach of phylogeography to explain the origin and maintenance of biodiversity. Finally, we stress the importance of natural history collections as sources of high-quality phenotypic data that span temporal and spatial axes.
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The emerging amphibian disease chytridiomycosis is caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd). Amphibian populations and species differ in susceptibility to Bd, yet we know ...surprisingly little about the genetic basis of this natural variation. MHC loci encode peptides that initiate acquired immunity in vertebrates, making them likely candidates for determining disease susceptibility. However, MHC genes have never been characterized in the context of chytridiomycosis. Here, we performed experimental Bd infections in laboratory-reared frogs collected from five populations that show natural variation in Bd susceptibility. We found that alleles of an expressed MHC class IIB locus associate with survival following Bd infection. Across populations, MHC heterozygosity was a significant predictor of survival. Within populations, MHC heterozygotes and individuals bearing MHC allele Q had a significantly reduced risk of death, and we detected a significant signal of positive selection along the evolutionary lineage leading to allele Q. Our findings demonstrate that immunogenetic variation affects chytridiomycosis survival under controlled experimental conditions, confirming that host genetic polymorphisms contribute to chytridiomycosis resistance.
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Amphibians have been affected globally by the disease chytridiomycosis, caused by the fungus Batrachochytrium dendrobatidis (Bd), and we are just now beginning to understand how immunogenetic ...variability contributes to disease susceptibility. Lineages of an expressed major histocompatibility complex (MHC) class II locus involved in acquired immunity are associated with chytridiomycosis susceptibility in controlled laboratory challenge assays. Here, we extend these findings to natural populations that vary both in exposure and response to Bd. We find that MHC alleles and supertypes associated with Bd survival in the field show a molecular signal of positive selection, while those associated with susceptibility do not, supporting the hypothesis that heritable Bd tolerance is rapidly evolving. We compare MHC supertypes to neutral loci to demonstrate where selection versus demography is shaping MHC variability. One population with Bd tolerance in nature shows a significant signal of directional selection for the same allele (allele Q) that was significantly associated with survival in an earlier laboratory study. Our findings indicate that selective pressure for Bd survival drives rapid immunogenetic adaptation in some natural populations, despite differences in environment and demography. Our field-based analysis of immunogenetic variation confirms that natural amphibian populations have the evolutionary potential to adapt to chytridiomycosis.
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Anthropogenic trade and development have broken down dispersal barriers, facilitating the spread of diseases that threaten Earth's biodiversity. We present a global, quantitative assessment of the ...amphibian chytridiomycosis panzootic, one of the most impactful examples of disease spread, and demonstrate its role in the decline of at least 501 amphibian species over the past half-century, including 90 presumed extinctions. The effects of chytridiomycosis have been greatest in large-bodied, range-restricted anurans in wet climates in the Americas and Australia. Declines peaked in the 1980s, and only 12% of declined species show signs of recovery, whereas 39% are experiencing ongoing decline. There is risk of further chytridiomycosis outbreaks in new areas. The chytridiomycosis panzootic represents the greatest recorded loss of biodiversity attributable to a disease.
Habitat loss and disease are main drivers of global amphibian declines, yet the interaction between them remains largely unexplored. Here we show that paradoxically, habitat loss is negatively ...associated with occurrence, prevalence, and infection intensity of the chytrid fungus Batrachochytrium dendrobatidis (Bd) in amphibian populations in the tropics. At a large spatial scale, increased habitat loss predicted lower disease risk in amphibian populations across Costa Rica and eastern Australia, even after jointly considering the effect of potential biotic and abiotic correlates. Lower host-species richness and suboptimal microclimates for Bd in disturbed habitats are potential mechanisms underlying this pattern. Furthermore, we found that anthropogenic deforestation practices biased to lowlands and natural vegetation remaining in inaccessible highlands explain increased Bd occurrence at higher elevations. At a smaller spatial scale, holding constant elevation, latitude, and macroclimate, we also found a negative relationship between habitat loss, and both Bd prevalence and infection intensity in frog populations in two landscapes of the Brazilian Atlantic Forest. Our results indicate that amphibians will be disproportionately affected by emerging diseases in pristine environments, and that, paradoxically, disturbed habitats may act as shelters from disease, but only for the very few species that can tolerate deforestation. Thus, tropical amphibian faunas are threatened both by destruction of natural habitats as well as increased disease in pristine forests. To curb further extinctions and develop effective mitigation and restoration programs we must look to interactions between habitat loss and disease, the two main factors at the root of global amphibian declines.
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Sexual dichromatism, a form of sexual dimorphism in which males and females differ in colour, is widespread in animals but has been predominantly studied in birds, fishes and butterflies. Moreover, ...although there are several proposed evolutionary mechanisms for sexual dichromatism in vertebrates, few studies have examined this phenomenon outside the context of sexual selection. Here, we describe unexpectedly high diversity of sexual dichromatism in frogs and create a comparative framework to guide future analyses of the evolution of these sexual colour differences. We review what is known about evolution of colour dimorphism in frogs, highlight alternative mechanisms that may contribute to the evolution of sexual colour differences, and compare them to mechanisms active in other major groups of vertebrates. In frogs, sexual dichromatism can be dynamic (temporary colour change in males) or ontogenetic (permanent colour change in males or females). The degree and the duration of sexual colour differences vary greatly across lineages, and we do not detect phylogenetic signal in the distribution of this trait, therefore frogs provide an opportunity to investigate the roles of natural and sexual selection across multiple independent derivations of sexual dichromatism.
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Genomic studies of the amphibian-killing fungus (Batrachochytrium dendrobatidis, Bd) identified three highly divergent genetic lineages, only one of which has a global distribution. Bd strains within ...these linages show variable genomic content due to differential loss of heterozygosity and recombination. The current quantitative polymerase chain reaction (qPCR) protocol to detect the fungus from amphibian skin swabs targets the intergenic transcribed spacer 1 (ITS1) region using a TaqMan fluorescent probe specific to Bd. We investigated the consequences of genomic differences in the quantification of ITS1 from eight distinct Bd strains, including representatives from North America, South America, the Caribbean, and Australia. To test for potential differences in amplification, we compared qPCR standards made from Bd zoospore counts for each strain, and showed that they differ significantly in amplification rates. To test potential mechanisms leading to strain differences in qPCR reaction parameters (slope and y-intercept), we: a) compared standard curves from the same strains made from extracted Bd genomic DNA in equimolar solutions, b) quantified the number of ITS1 copies per zoospore using a standard curve made from PCR-amplicons of the ITS1 region, and c) cloned and sequenced PCR-amplified ITS1 regions from these same strains to verify the presence of the probe site in all haplotypes. We found high strain variability in ITS1 copy number, ranging from 10 to 144 copies per single zoospore. Our results indicate that genome size might explain strain differences in ITS1 copy number, but not ITS1 sequence variation because the probe-binding site and primers were conserved across all haplotypes. For standards constructed from uncharacterized Bd strains, we recommend the use of single ITS1 PCR-amplicons as the absolute standard in conjunction with current quantitative assays to inform on copy number variation and provide universal estimates of pathogen zoospore loads from field-caught amphibians.
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Species richness is greatest in the tropics, and much of this diversity is concentrated in mountains. Janzen proposed that reduced seasonal temperature variation selects for narrower thermal ...tolerances and limited dispersal along tropical elevation gradients Janzen DH (1967) Am Nat 101:233–249. These locally adapted traits should, in turn, promote reproductive isolation and higher speciation rates in tropical mountains compared with temperate ones. Here, we show that tropical and temperate montane stream insects have diverged in thermal tolerance and dispersal capacity, two key traits that are drivers of isolation in montane populations. Tropical species in each of three insect clades have markedly narrower thermal tolerances and lower dispersal than temperate species, resulting in significantly greater population divergence, higher cryptic diversity, higher tropical speciation rates, and greater accumulation of species over time. Our study also indicates that tropical montane species, with narrower thermal tolerance and reduced dispersal ability, will be especially vulnerable to rapid climate change.
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Naive multi-host communities include species that may differentially maintain, transmit and amplify novel pathogens; therefore, we expect species to fill distinct roles during infectious disease ...emergence. Characterizing these roles in wildlife communities is challenging because most disease emergence events are unpredictable. Here, we used field-collected data to investigate how species-specific attributes influenced the degree of exposure, probability of infection, and pathogen intensity, during the emergence of the fungal pathogen
(
) in a highly diverse tropical amphibian community. Our findings confirmed that ecological traits commonly evaluated as correlates of decline were positively associated with infection prevalence and intensity at the species level during the outbreak. We identified key hosts that disproportionally contributed to transmission dynamics in this community and found a signature of phylogenetic history in disease responses associated with increased pathogen exposure via shared life-history traits. Our findings establish a framework that could be applied in conservation efforts to identify key species driving disease dynamics under enzootics before reintroducing amphibians back into their original communities. Reintroductions of supersensitive hosts that are unable to overcome infections will limit the success of conservation programmes by amplifying the disease at the community level. This article is part of the theme issue 'Amphibian immunity: stress, disease and ecoimmunology'.
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