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Abstract Populations along steep environmental gradients are subject to differentiating selection that can result in local adaptation, despite countervailing gene flow, and genetic drift. In montane systems, where species are often restricted to narrow ranges of elevation, it is unclear whether the selection is strong enough to influence functional differentiation of subpopulations differing by a few hundred meters in elevation. We used targeted capture of 12 501 exons from across the genome, including 271 genes previously implicated in altitude adaptation, to test for adaptation to local elevations for 2 highland hummingbird species, Coeligena violifer (n = 62) and Colibri coruscans (n = 101). For each species, we described population genetic structure across the complex geography of the Peruvian Andes and, while accounting for this structure, we tested whether elevational allele frequency clines in single nucleotide polymorphisms (SNPs) showed evidence for local adaptation to elevation. Although the 2 species exhibited contrasting population genetic structures, we found signatures of clinal genetic variation with shifts in elevation in both. The genes with SNP-elevation associations included candidate genes previously discovered for high-elevation adaptation as well as others not previously identified, with cellular functions related to hypoxia response, energy metabolism, and immune function, among others. Despite the homogenizing effects of gene flow and genetic drift, natural selection on parts of the genome evidently optimizes elevation-specific cellular function even within elevation range-restricted montane populations. Consequently, our results suggest local adaptation occurring in narrow elevation bands in tropical mountains, such as the Andes, may effectively make them “taller” biogeographic barriers. 

Understanding the genetic basis of environmental adaptation in natural populations is a central goal in evolutionary biology. The conditions at high elevation, particularly the low oxygen available in the ambient air, impose a significant and chronic environmental challenge to metabolically active animals with lowland ancestry. To understand the process of adaptation to these novel conditions and to assess the repeatability of evolution over short timescales, we examined the signature of selection from complete exome sequences of house mice (Mus musculus domesticus) sampled across two elevational transects in the Andes of South America. Using phylogenetic analysis, we show that house mice colonized high elevations independently in Ecuador and Bolivia. Overall, we found distinct responses to selection in each transect and largely nonoverlapping sets of candidate genes, consistent with the complex nature of traits that underlie adaptation to low oxygen availability (hypoxia) in other species. Nonetheless, we also identified a small subset of the genome that appears to be under parallel selection at the gene and SNP levels. In particular, three genes (Col22a1, Fgf14, and srGAP1) bore strong signatures of selection in both transects. Finally, we observed several patterns that were common to both transects, including an excess of derived alleles at high elevation, and a number of hypoxia-associated genes exhibiting a threshold effect, with a large allele frequency change only at the highest elevations. This threshold effect suggests that selection pressures may increase disproportionately at high elevations in mammals, consistent with observations of some high-elevation diseases in humans.

 

Abstract Understanding diversity has been a pursuit in evolutionary biology since its inception. A challenge arises when sexual selection has played a role in diversification. Questions of what constitutes a ‘species’, homoplasy vs. synapomorphy, and whether sexually selected traits show phylogenetic signal have hampered work on many systems. Peacock spiders are famous for sexually selected male courtship dances and peacock-like abdominal ornamentation. This lineage of jumping spiders currently includes over 90 species classified into two genera, Maratus and Saratus. Most Maratus species have been placed into groups based on secondary sexual characters, but evolutionary relationships remain unresolved. Here we assess relationships in peacock spiders using phylogenomic data (ultraconserved elements and RAD-sequencing). Analyses reveal that Maratus and the related genus Saitis are paraphyletic. Many, but not all, morphological groups within a ‘core Maratus’ clade are recovered as genetic clades but we find evidence for undocumented speciation. Based on original observations of male courtship, our comparative analyses suggest that courtship behaviour and peacock-like abdominal ornamentation have evolved sequentially, with some traits inherited from ancestors and others evolving repeatedly and independently from ‘simple’ forms. Our results have important implications for the taxonomy of these spiders, and provide a much-needed evolutionary framework for comparative studies of the evolution of sexual signal characters. 

Penguins are the only extant family of flightless diving birds. They currently comprise at least 18 species, distributed from polar to tropical environments in the Southern Hemisphere. The history of their diversification and adaptation to these diverse environments remains controversial. We used 22 new genomes from 18 penguin species to reconstruct the order, timing, and location of their diversification, to track changes in their thermal niches through time, and to test for associated adaptation across the genome. Our results indicate that the penguin crown-group originated during the Miocene in New Zealand and Australia, not in Antarctica as previously thought, and thatAptenodytesis the sister group to all other extant penguin species. We show that lineage diversification in penguins was largely driven by changing climatic conditions and by the opening of the Drake Passage and associated intensification of the Antarctic Circumpolar Current (ACC). Penguin species have introgressed throughout much of their evolutionary history, following the direction of the ACC, which might have promoted dispersal and admixture. Changes in thermal niches were accompanied by adaptations in genes that govern thermoregulation and oxygen metabolism. Estimates of ancestral effective population sizes (N_e) confirm that penguins are sensitive to climate shifts, as represented by three different demographic trajectories in deeper time, the most common (in 11 of 18 penguin species) being an increasedN_ebetween 40 and 70 kya, followed by a precipitous decline during the Last Glacial Maximum. The latter effect is most likely a consequence of the overall decline in marine productivity following the last glaciation.

 

The diversification of a host lineage can be influenced by both the external environment and its assemblage of microbes. Here, we use a young lineage of spiders, distributed along a chronologically arranged series of volcanic mountains, to investigate how their associated microbial communities have changed as the spiders colonized new locations. Using the stick spiderAriamnes waikula(Araneae, Theridiidae) on the island of Hawaiʻi, and outgroup taxa on older islands, we tested whether each component of the “holobiont” (spider hosts, intracellular endosymbionts and gut microbial communities) showed correlated signatures of diversity due to sequential colonization from older to younger volcanoes. To investigate this, we generated ddRAD data for the host spiders and 16S rRNA gene amplicon data from their microbiota. We expected sequential colonizations to result in a (phylo)genetic structuring of the host spiders and in a diversity gradient in microbial communities. The results showed that the hostA.waikulais indeed structured by geographical isolation, suggesting sequential colonization from older to younger volcanoes. Similarly, the endosymbiont communities were markedly different betweenAriamnesspecies on different islands, but more homogeneous amongA.waikulapopulations on the island of Hawaiʻi. Conversely, the gut microbiota, which we suspect is generally environmentally derived, was largely conserved across all populations and species. Our results show that different components of the holobiont respond in distinct ways to the dynamic environment of the volcanic archipelago. This highlights the necessity of understanding the interplay between different components of the holobiont, to properly characterize its evolution.

 

Avoiding extinction in a rapidly changing environment often relies on a species’ ability to quickly adapt in the face of extreme selective pressures. In Panamá, two closely related harlequin frog species (Atelopus variusandAtelopus zeteki) are threatened with extinction due to the fungal pathogenBatrachochytrium dendrobatidis(Bd). Once thought to be nearly extirpated from Panamá,A. variushave recently been rediscovered in multiple localities across their historical range; however,A. zetekiare possibly extinct in the wild. By leveraging a unique collection of 186Atelopustissue samples collected before and after theBdoutbreak in Panama, we describe the genetics of persistence for these species on the brink of extinction. We sequenced the transcriptome and developed an exome‐capture assay to sequence the coding regions of theAtelopusgenome. Using these genetic data, we evaluate the population genetic structure of historicalA. variusandA. zetekipopulations, describe changes in genetic diversity over time, assess the relationship between contemporary and historical individuals, and test the hypothesis that someA. variuspopulations have rapidly evolved to resist or tolerateBdinfection. We found a significant decrease in genetic diversity in contemporary (compared to historical)A. variuspopulations. We did not find strong evidence of directional allele frequency change or selection forBdresistance genes, but we uncovered a set of candidate genes that warrant further study. Additionally, we found preliminary evidence of recent migration and gene flow in one of the largest persistingA. variuspopulations in Panamá, suggesting the potential for genetic rescue in this system. Finally, we propose that previous conservation units should be modified, as clear genetic breaks do not exist beyond the local population level. Our data lay the groundwork for genetically informed conservation and advance our understanding of how imperiled species might be rescued from extinction.

 

Identifying a common set of genes that mediate host–microbial interactions across populations and species of mammals has broad relevance for human health and animal biology. However, the genetic basis of the gut microbial composition in natural populations remains largely unknown outside of humans. Here, we used wild house mouse populations as a model system to ask three major questions: (a) Does host genetic relatedness explain interindividual variation in gut microbial composition? (b) Do population differences in the microbiota persist in a common environment? (c) What are the host genes associated with microbial richness and the relative abundance of bacterial genera? We found that host genetic distance is a strong predictor of the gut microbial composition as characterized by 16S amplicon sequencing. Using a common garden approach, we then identified differences in microbial composition between populations that persisted in a shared laboratory environment. Finally, we used exome sequencing to associate host genetic variants with microbial diversity and relative abundance of microbial taxa in wild mice. We identified 20 genes that were associated with microbial diversity or abundance including a macrophage‐derived cytokine (IL12a) that contained three nonsynonymous mutations. Surprisingly, we found a significant overrepresentation of candidate genes that were previously associated with microbial measurements in humans. The homologous genes that overlapped between wild mice and humans included genes that have been associated with traits related to host immunity and obesity in humans. Gene–bacteria associations identified in both humans and wild mice suggest some commonality to the host genetic determinants of gut microbial composition across mammals.

 

The Lesser Sunda Islands are situated between the Sunda and Sahul Shelves, with a linear arrangement that has functioned as a two‐way filter for taxa dispersing between the Asian and Australo‐Papuan biogeographical realms. Distributional patterns of many terrestrial vertebrates suggest a stepping‐stone model of island colonization. Here we investigate the timing and sequence of island colonization in Asian‐origin fanged frogs from the volcanic Sunda Arc islands with the goal of testing the stepping‐stone model of island colonization.

The Indonesian islands of Java, Lombok, Sumbawa, Flores and Lembata.

Limnonectes dammermaniandL. kadarsani(Family: Dicroglossidae)

MitochondrialDNAwas sequenced from 153 frogs to identify major lineages and to select samples for an exon‐capture experiment. We designed probes to capture sequence data from 974 exonic loci (1,235,981 bp) from 48 frogs including the outgroup species,L. microdiscus. The resulting data were analysed using phylogenetic, population genetic and biogeographical model testing methods.

The mtDNAphylogeny findsL. kadarsaniparaphyletic with respect toL. dammermani, with a pectinate topology consistent with the stepping‐stone model. Phylogenomic analyses of 974 exons recovered the two species as monophyletic sister taxa that diverged ~7.6 Ma with no detectable contemporary gene flow, suggesting introgression of theL. dammermanimitochondrion intoL. kadarsanion Lombok resulting from an isolated ancient hybridization event ~4 Ma. WithinL. kadarsani,the Lombok lineage diverged first while the Sumbawa and Lembata lineages are nested within a Flores assemblage composed of two parapatrically distributed lineages meeting in central Flores. Biogeographical model comparison found strict stepping‐stone dispersal to be less likely than models involving leap‐frog dispersal events.

These results suggest that the currently accepted stepping‐stone model of island colonization might not best explain the current patterns of diversity in the archipelago. The high degree of genetic structure, large divergence times, and absent or low levels of migration between lineages suggests thatL. kadarsanirepresents five distinct species.