Host, microbiome, and complex space: applying population and landscape genetic approaches to gut microbiome research in wild populations

In recent years, emerging sequencing technologies and computational tools have driven a tidal wave of research on host-associated microbiomes, particularly the gut microbiome. These studies demonstrate numerous connections between the gut microbiome and vital host functions, primarily in humans, model organisms, and domestic animals. As the adaptive importance of the gut microbiome becomes clearer, interest in studying the gut microbiomes of wild populations has increased, in part due to the potential for discovering conservation applications. The study of wildlife gut microbiomes holds many new challenges and opportunities due to the complex genetic, spatial, and environmental structure of wild host populations, and the potential for these factors to interact with the microbiome. The emerging picture of adaptive coevolution in host-microbiome relationships highlights the importance of understanding microbiome variation in the context of host population genetics and landscape heterogeneity across a wide range of host populations. We propose a conceptual framework for understanding wildlife gut microbiomes in relation to landscape variables and host population genetics, including the potential of approaches derived from landscape genetics. We use this framework to review current research, synthesize important trends, highlight implications for conservation, and recommend future directions for research. Specifically, we focus on how spatial structure and environmental variation interact with host population genetics and microbiome variation in natural populations, and what we can learn from how these patterns of covariation differ depending on host ecological and evolutionary traits.

Holo-Transcriptome Sequences from the Tropical Marine Sponge Cinachyrella alloclada

Marine sponge transcriptomes are underrepresented in current databases. Furthermore, only two sponge genomes are available for comparative studies. Here we present the assembled and annotated holo-transcriptome of the common Florida reef sponge from the species Cinachyrella alloclada. After Illumina high throughput sequencing, the data assembled using Trinity v2.5 confirmed a highly symbiotic organism, with the complexity of high microbial abundance (HMA) sponges. This dataset is enriched in poly-A selected eukaryotic, rather than microbial transcripts. Overall, 39,813 transcripts with verified sponge sequence homology coded for 8,496 unique proteins. The average sequence length was found to be 946 bp with an N50 sequence length of 1290 bp. Overall, the sponge assembly resulted in a GC content of 51.04%, which is within the range of GC bases in a eukaryotic transcriptome. BUSCO scored completeness analysis revealed a completeness of 60.3% and 60.1% based on the Eukaryota and Metazoa databases, respectively. Overall, this study points to an overarching goal of developing the Cinachyrella alloclada sponge as a useful new experimental model organism.

Temporal analysis of effective population size and mating system in a social wasp

Highly social species are successful because they cooperate in obligately integrated societies. We examined temporal genetic variation in the eusocial wasp Vespula maculifrons in order to gain a greater understanding of evolution in highly social taxa. First, we wished to test if effective population sizes of eusocial species were relatively low due to the reproductive division of labor that characterizes eusocial taxa. We thus estimated the effective population size of V. maculifrons by examining temporal changes in population allele frequencies. We sampled the genetic composition of a V. maculifrons population at three separate time points spanning a 13-year period. We found that effective population size ranged in the hundreds of individuals, which is similar to estimates in other, non-eusocial taxa. Second, we estimated levels of polyandry in V. maculifrons in different years in order to determine if queen mating system varied over time. We found no significant change in the number or skew of males mated to queens. In addition, mating skew was not significant within V. maculifrons colonies. Therefore, our data suggest that queen mate number may be subject to stabilizing selection in this taxon. Overall, our study provides novel insight into the selective processes operating in eusocial species by analyzing temporal genetic changes within populations.

Ancient introgression between distantly related white oaks (Quercus sect Quercus) shows evidence of climate-associated asymmetric gene exchange

Ancient introgression can be an important source of genetic variation that shapes the evolution and diversification of many taxa. Here, we estimate the timing, direction and extent of gene flow between two distantly related oak species in the same section (Quercus sect. Quercus). We estimated these demographic events using genotyping by sequencing data (GBS), which generated 25,702 single nucleotide polymorphisms (SNPs) for 24 individuals of California scrub oak (Quercus berberidifolia) and 23 individuals of Engelmann oak (Q. engelmannii). We tested several scenarios involving gene flow between these species using the diffusion approximation-based population genetic inference framework and model-testing approach of the Python package DaDi. We found that the most likely demographic scenario includes a bottleneck in Q. engelmannii that coincides with asymmetric gene flow from Q. berberidifolia into Q. engelmannii. Given that the timing of this gene flow coincides with the advent of a Mediterranean-type climate in the California Floristic Province, we propose that changing precipitation patterns and seasonality may have favored the introgression of climate-associated genes from the endemic into the non-endemic California oak.

Variable signatures of selection despite conserved recombination landscapes early in speciation

Recently diverged taxa often exhibit heterogeneous landscapes of genomic differentiation, characterized by regions of elevated differentiation on an otherwise homogeneous background. While divergence peaks are generally interpreted as regions responsible for reproductive isolation, they can also arise due to background selection, selective sweeps unrelated to speciation, and variation in recombination and mutation rates. To investigate the association between patterns of recombination and landscapes of genomic differentiation during the early stages of speciation, we generated fine-scale recombination maps for six southern capuchino seedeaters (Sporophila) and two subspecies of White Wagtail (Motacilla alba), two recent avian radiations in which divergent selection on pigmentation genes has likely generated peaks of differentiation. We compared these recombination maps to those of Collared (Ficedula albicollis) and Pied Flycatchers (Ficedula hypoleuca), non-sister taxa characterized by moderate genomic divergence and a heterogenous landscape of genomic differentiation shaped in part by background selection. Although recombination landscapes were conserved within all three systems, we documented a weaker negative correlation between recombination rate and genomic differentiation in the recent radiations. All divergence peaks between capuchinos, wagtails, and flycatchers were located in regions with lower-than-average recombination rates, and most divergence peaks in capuchinos and flycatchers fell in regions of exceptionally reduced recombination. Thus, co-adapted allelic combinations in these regions may have been protected early in divergence, facilitating rapid diversification. Despite largely conserved recombination landscapes, divergence peaks are specific to each focal comparison in capuchinos, suggesting that regions of elevated differentiation have not been generated by variation in recombination rate alone.

Sperm Storage in a Family-Living Lizard, the Tree Skink (Egernia striolata)

The ability to produce viable offspring without recently mating, either through sperm storage or parthenogenesis, can provide fitness advantages under a suite of challenging ecological scenarios. Using genetic analysis, we demonstrate that three wild-caught female Tree Skinks (Egernia striolata) reproduced in captivity with no access to males for over a year, and that this is best explained by sperm storage. To the best of our knowledge, this is the first time female sperm storage has been documented in any monogamous family-living reptile, including social Australian egerniine skinks (from the subfamily Egerniinae). Furthermore, by using paternal reconstruction of genotypes we show that captive-born offspring produced by the same females in the preceding year, presumably without sperm storage, were sired by different males. We qualitatively compared aspects of these females’ mates and offspring between years. The parents of each litter were unrelated, but paternal and offspring genotypes from litters resulting from stored sperm were more heterozygous than those inferred to be from recent matings. Family-living egerniine skinks generally have low rates of multiple paternity, yet our study suggests that female sperm storage, potentially from outside social partners, offers the real possibility of benefits. Possible benefits include increasing genetic compatibility of mates and avoiding inbreeding depression via cryptic female choice. Sperm storage in Tree Skinks, a family-living lizard with a monogamous mating system, suggests that females may bet-hedge through extra-pair copulation with more heterozygous males, reinforcing the idea that females could have more control on reproductive outcomes than previously thought.