Papers will be added with the newest at the top. Current preprints (not yet peer-reviewed) are available here.
Rigorous science demands support of transgender scientists
K Aghi, BM Anderson, BM Castellano, A Cunningham, M Delano, ES Dickinson, L von Diezmann, SK Forslund-Startceva, DM Grijseels, SS Groh, EM Guthman, I Jayasinghe, J Johnston, S Long, JF McLaughlin, M McLaughlin, M Miyagi, B Rajaraman, F Sancheznieto. AI Scheim, SD Sun, FD Titmuss, RJ Walsh, ZY Weinberg
Abstract:
To build a just, equitable, and diverse academy, scientists and institutions must address systemic barriers that sex and gender minorities face. This Commentary summarizes (1) critical context informing the contemporary oppression of transgender people, (2) how this shapes extant research on sex and gender, and (3) actions to build an inclusive and rigorous academy for all.
A lack of genetic diversity and minimal adaptive evolutionary divergence in introduced Mysis shrimp after 50 years
RG Cheek, JF McLaughlin, MP Gamboa, CA Marshall, BM Johnson, DB Silver, AA Mauro, CK Ghalambor
Abstract:
The successes of introduced populations in novel habitats often provide powerful examples of evolution and adaptation. In the 1950s, opossum shrimp (Mysis diluviana) individuals from Clearwater Lake in Minnesota, USA were transported and introduced to Twin Lakes in Colorado, USA by fisheries managers to supplement food sources for trout. Mysis were subsequently introduced from Twin Lakes into numerous lakes throughout Colorado. Because managers kept detailed records of the timing of the introductions, we had the opportunity to test for evolutionary divergence within a known time interval. Here, we used reduced representation genomic data to investigate patterns of genetic diversity, test for genetic divergence between populations, and for evidence of adaptive evolution within the introduced populations in Colorado. We found very low levels of genetic diversity across all populations, with evidence for some genetic divergence between the Minnesota source population and the introduced populations in Colorado. There was little differentiation among the Colorado populations, consistent with the known provenance of a single founding population, with the exception of the population from Gross Reservoir, Colorado. Demographic modeling suggests that at least one undocumented introduction from an unknown source population hybridized with the population in Gross Reservoir. Despite the overall low genetic diversity we observed, FST outlier and environmental association analyses identified multiple loci exhibiting signatures of selection and adaptive variation related to elevation and lake depth. The success of introduced species is thought to be limited by genetic variation, but our results imply that populations with limited genetic variation can become established in a wide range of novel environments. From an applied perspective, the observed patterns of divergence between populations suggest that genetic analysis can be a useful forensic tool to determine likely sources of invasive species.
Sex and biology: broader impacts beyond the binary
SL Sharpe, AP Anderson, I Cooper, TY James, AE Kralick, H Lindahl, SE Lipshutz, JF McLaughlin, B Subramaniam, AR Weigel, AK Lewis
Abstract:
What are the implications of misunderstanding sex as a binary, and why is it essential for scientists to incorporate a more expansive view of biological sex in our teaching and research? This roundtable will include many of our symposium speakers, including biologists and intersex advocates, to discuss these topics and visibilize the link between ongoing reification of dyadic sex within scientific communities and the social, political, and medical oppression faced by queer, transgender, and especially intersex communities. As with the symposium as a whole, this conversation is designed to bring together empirical research and implementation of equity, inclusion, and justice principles, which are often siloed into separate rooms and conversations at academic conferences. Given the local and national attacks on the rights of intersex individuals and access to medical care and bodily autonomy, this interdisciplinary discussion is both timely and urgent.
Multivariate models of animal sex: breaking binaries leads to a better understanding of ecology and evolution
JF McLaughlin, KM Brock, I Gates, A Pethkar, M Piattoni, A Rossi, SE Lipshutz
Abstract:
‘Sex’ is often used to describe a suite of phenotypic and genotypic traits of an organism related to reproduction. However, these traits – gamete type, chromosomal inheritance, physiology, morphology, behavior, etc. – are not necessarily coupled, and the rhetorical collapse of variation into a single term elides much of the complexity inherent in sexual phenotypes. We argue that consideration of ‘sex’ as a constructed category operating at multiple biological levels opens up new avenues for inquiry in our study of biological variation. We apply this framework to three case studies that illustrate the diversity of sex variation, from decoupling sexual phenotypes to the evolutionary and ecological consequences of intrasexual polymorphisms. We argue that instead of assuming binary sex in these systems, some may be better categorized as multivariate and nonbinary. Finally, we conduct a meta-analysis of terms used to describe diversity in sexual phenotypes in the scientific literature to highlight how a multivariate model of sex can clarify, rather than cloud, studies of sexual diversity within and across species. We argue that such an expanded framework of ‘sex’ better equips us to understand evolutionary processes, and that as biologists it is incumbent upon us to push back against misunderstandings of the biology of sexual phenotypes that enact harm on marginalized communities.
Figure 2. Mechanisms of sex determination vary widely across animals. The most familiar (top row) are the relatively simple (A) XX/XY (in purple, here shown with northern elephant seal, Mirounga angustirostris, as an example taxon) and (B) ZZ/ZW (in green, shown with royal flycatcher, Onychorhynchus coronatus). (C) Haplodiploid sex determination involves sex being determined by having one or two copies of the genome, and is found predominantly in insects such as the pictured Dasymutilla occidentalis. (D) A mutation in the X chromosome of some African pygmy mice (Mus minutoides) overrides the presence of a Y chromosome, and (E) in some cichlids (shown here with Metriaclima mbenjii), both the absence of the W chromosome and presence of the Y are required for an individual to develop 'male' characteristics. (F) In central bearded dragons (Pogona vitticeps), the ZZ genotype is overridden by high temperatures, leading to phenotypically 'female' individuals capable of laying eggs. (G) The white-throated sparrow (Zonotrichia albicollis) is found in two color morphs linked to a large inversion on chromosome two (in turquoise), which is paired with the Z and W genotype to determine which individuals typically reproduce with each other.
Figure 1. Distribution of samples used in this study, focusing on Beringia and South America (inset). A. c. crecca occurs throughout most of Eurasia and seasonally migrates through the western Aleutians (light blue; 6 individuals), A. c. nimia occurs as a resident in the Aleutian Islands (dark blue; 3 individuals), and A. c. carolinensis occurs across North America (gold; 7 individuals). The yellow-billed teal, Anas flavirostris (red; 4 individuals) is a South American sister taxon; our samples include two members of this superspecies complex, A. [f.] flavirostris and A. [f.] andium. See Supplementary Table S1 for specimen details. Illustration of green-winged teal courtesy of USFWS (Hines, 1963).
Population genomics indicate three different modes of divergence and speciation with gene flow in the green-winged teal duck complex
F Spaulding, JF McLaughlin, RG CHeek, KG McCracken, TC Glenn, K Winker
Abstract:
The processes leading to divergence and speciation can differ broadly among taxa with different life histories. We examine these processes in a small clade of ducks with historically uncertain relationships and species limits. The green-winged teal (Anas crecca) complex is a Holarctic species of dabbling duck currently categorized as three subspecies (Anas crecca crecca, A. c. nimia, and A. c. carolinensis) with a close relative, the yellow-billed teal (Anas flavirostris) from South America. A. c. crecca and A. c. carolinensis are seasonal migrants, while the other taxa are sedentary. We examined divergence and speciation patterns in this group, determining their phylogenetic relationships and the presence and levels of gene flow among lineages using both mitochondrial and genome-wide nuclear DNA obtained from 1,393 ultraconserved element (UCE) loci. Phylogenetic relationships using nuclear DNA among these taxa showed A. c. crecca, A. c. nimia, and A. c. carolinensis clustering together to form one polytomous clade, with A. flavirostris sister to this clade. This relationship can be summarized as (crecca, nimia, carolinensis)(flavirostris). However, whole mitogenomes revealed a different phylogeny: (crecca, nimia)(carolinensis, flavirostris). The best demographic model for key pairwise comparisons supported divergence with gene flow as the probable speciation mechanism in all three contrasts (crecca─nimia, crecca─carolinensis, and carolinensis─flavirostris). Given prior work, gene flow was expected among the Holarctic taxa, but gene flow between North American carolinensis and South American flavirostris (M ∼0.1 - 0.4 individuals/generation), albeit low, was not expected. Three geographically oriented modes of divergence are likely involved in the diversification of this complex: heteropatric (crecca─nimia), parapatric (crecca─carolinensis), and (mostly) allopatric (carolinensis─flavirostris). Our study shows that ultraconserved elements are a powerful tool for simultaneously studying systematics and population genomics in systems with historically uncertain relationships and species limits.
Estimating movement rates between Eurasian and North American birds that are vectors of avian influenza
F Spaulding, JF McLaughlin, TC Glenn, K WInker
Abstract:
Avian influenza (AI) is a zoonotic disease that will likely be involved in future pandemics. Because waterbird movements are difficult to quantify, determining the host-specific risk of Eurasian-origin AI movements into North America is challenging. We estimated relative rates of movements, based on long-term evolutionary averages of gene flow, between Eurasian and North American waterbird populations to obtain bidirectional baseline rates of the intercontinental movements of these AI hosts. We used population genomics and coalescent-based demographic models to obtain these gene-flow–based movement estimates. Inferred rates of movement between these continental populations varies greatly among species. Within dabbling ducks, gene flow, relative to effective population size, varies from ∼3 to 24 individuals/generation between Eurasian and American wigeons (Mareca penelope and Mareca americana) to ∼100–300 individuals/generation between continental populations of northern pintails (Anas acuta). These are evolutionary long-term averages and provide a solid foundation for understanding the relative risks of each of these host species in potential intercontinental AI movements. We scale these values to census size for evaluation in that context. In addition to being AI hosts, many of these bird species are also important in the subsistence diets of Alaskans, increasing the risk of direct bird-to-human exposure to Eurasian-origin AI virus. We contrast species-specific rates of intercontinental movements with the importance of each species in Alaskan diets to understand the relative risk of these taxa to humans. Assuming roughly equivalent AI infection rates among ducks, greater scaup (Aythya marila), mallard (Anas platyrhynchos), and northern pintail (Anas acuta) were the top three species presenting the highest risks for intercontinental AI movement both within the natural system and through exposure to subsistence hunters. Improved data on AI infection rates in this region could further refine these relative risk assessments. These directly comparable, species-based intercontinental movement rates and relative risk rankings should help in modeling, monitoring, and mitigating the impacts of intercontinental host and AI movements.
Pitfall traps from NEON Macrosystems project. Photo: JFM
Robust metagenomic evidence that local assemblage richness increases with latitude in ground-active invertebrates of North America
M Weiser, C Siler, SN Smith KE Marshall, JF McLaughlin, MJ Miller, M Kaspari
Abstract:
Biodiversity monitoring is imperative for understanding how changing climate may impact the distributions of taxa from single species to the spatial distribution of biological diversity. Large-scale and cross-taxa biodiversity monitoring also allows an empirical understanding of biogeographic patterns across taxa. One such pattern, where in taxonomic richness peaks at tropical latitudes are typically treated as a biogeographical rule with few notable exceptions. Here we leveraged the invertebrate pitfall collections of the National Ecological Observatory Network (NEON) across North America to describe patterns of local taxonomic richness across taxa and across taxonomic scale. We focused on Arthropoda, Annelida and Mollusca. Additionally, we estimated regional species richness using expert-identified samples of three NEON sentinel taxa: Carabidae, Culicidae and Ixodida. To sample pitfall animals, we filtered storage ethanol and employed environmental DNA-barcoding methodologies to amplify and sequence extracted DNA from the filtrate for two regions of a mitochondrial gene. We assigned taxonomic names to these sequences at 97% similarity to reference sequences and calculated local taxonomic richness at the levels of species, genus, family and order. We calculated local species richness for 12 common invertebrate taxa. We used generalized linear models to describe the relationships between taxonomic richness and spatial, climatic and abundance predictor variables. At four taxonomic scales, ranging from species to order, taxonomic richness increased significantly as a function of latitude. Of the twelve invertebrate taxa we examined, seven mirrored this positive latitudinal gradient in species richness. At the regional scale, two of three NEON Sentinel Taxa showed positive latitudinal gradients in species richness. Temperature, precipitation, abundance and sequence read number played minor roles in explaining patterns of taxonomic richness. When considering these mostly temperate sites that span 46 degrees of latitude, we found no support for the expected negative latitudinal gradients across taxa and taxonomic scales. Instead, for many of these taxa and taxonomic scales, we observed significant, positive richness gradients with increasing latitude among ground-dwelling invertebrate communities. Thus, one of the most ‘general’ patterns in biogeography was not found for most invertebrate taxa across temperate latitudes.
An empirical examination of sample size effects on population demographic estimates in birds using single nucleotide polymorphism (SNP) data
JF McLaughlin, K Winker
Abstract:
Sample size is a critical aspect of study design in population genomics research, yet few empirical studies have examined the impacts of small sample sizes. We used datasets from eight diverging bird lineages to make pairwise comparisons at different levels of taxonomic divergence (populations, subspecies, and species). Our data are from loci linked to ultraconserved elements and our analyses used one single nucleotide polymorphism per locus. All individuals were genotyped at all loci, effectively doubling sample size for coalescent analyses. We estimated population demographic parameters (effective population size, migration rate, and time since divergence) in a coalescent framework using Diffusion Approximation for Demographic Inference, an allele frequency spectrum method. Using divergence-with-gene-flow models optimized with full datasets, we subsampled at sequentially smaller sample sizes from full datasets of 6–8 diploid individuals per population (with both alleles called) down to 1:1, and then we compared estimates and their changes in accuracy. Accuracy was strongly affected by sample size, with considerable differences among estimated parameters and among lineages. Effective population size parameters (ν) tended to be underestimated at low sample sizes (fewer than three diploid individuals per population, or 6:6 haplotypes in coalescent terms). Migration (m) was fairly consistently estimated until <2 individuals per population, and no consistent trend of over-or underestimation was found in either time since divergence (T) or theta (Θ = 4Nrefμ). Lineages that were taxonomically recognized above the population level (subspecies and species pairs; that is, deeper divergences) tended to have lower variation in scaled root mean square error of parameter estimation at smaller sample sizes than population-level divergences, and many parameters were estimated accurately down to three diploid individuals per population. Shallower divergence levels (i.e., populations) often required at least five individuals per population for reliable demographic inferences using this approach. Although divergence levels might be unknown at the outset of study design, our results provide a framework for planning appropriate sampling and for interpreting results if smaller sample sizes must be used.
Divergence, gene flow, and speciation in eight lineages of trans-Beringian birds
JF McLaughlin, BC Faircloth, TC Glenn, K Winker
Abstract:
Determining how genetic diversity is structured between populations that span the divergence continuum from populations to biological species is key to understanding the generation and maintenance of biodiversity. We investigated genetic divergence and gene flow in eight lineages of birds with a trans‐Beringian distribution, where Asian and North American populations have likely been split and reunited through multiple Pleistocene glacial cycles. Our study transects the speciation process, including eight pairwise comparisons in three orders (ducks, shorebirds, and passerines) at population, subspecies, and species levels. Using ultraconserved elements (UCEs), we found that these lineages represent conditions from slightly differentiated populations to full biological species. Although allopatric speciation is considered the predominant mode of divergence in birds, all of our best divergence models included gene flow, supporting speciation with gene flow as the predominant mode in Beringia. In our eight lineages, three were best described by a split‐migration model (divergence with gene flow), three best fit a secondary‐contact scenario (isolation followed by gene flow), and two showed support for both models. The lineages were not evenly distributed across a divergence space defined by gene flow (M ) and differentiation (FST ), instead forming two discontinuous groups: one with relatively shallow divergence, no fixed SNPs, and high rates of gene flow between populations; and the second with relatively deeply divergent lineages, multiple fixed SNPs, and low gene flow. Our results highlight the important role that gene flow plays in avian divergence in Beringia.
A preliminary bird list from Río Luis, Veraguas province, provides further insight into an avian suture zone in Caribbean Panama
JF McLaughlin, JL Garzón, OG López Ch., MJ Miller
A Royal Flycatcher (Onychorhynchus coronatus) captured in July 2018 during Veraguas fieldwork. Photo: JF McLaughlin
Speciation, gene flow, and seasonal migration in Catharus thrushes (Aves:Turdidae)
KE Everson, JF McLaughlin, IA Cato, MM Evans, AR Gastaldi, KK Mills, KG Shink, SM Wilbur, K Winker
Abstract:
New World thrushes in the genus Catharus are small, insectivorous or omnivorous birds that have been used to explore several important questions in avian evolution, including the evolution of seasonal migration and plumage variation. Within Catharus, members of a clade of obligate long-distance migrants (C. fuscescens, C. minimus, and C. bicknelli) have also been used in the development of heteropatric speciation theory, a divergence process in which migratory lineages (which might occur in allopatry or sympatry during portions of their annual cycle) diverge despite low levels of gene flow. However, research on Catharus relationships has thus far been restricted to the use of small genetic datasets, which provide limited resolution of both phylogenetic and demographic histories. We used a large, multi-locus dataset from loci containing ultraconserved elements (UCEs) to study the demographic histories of the migratory C. fuscescens-minimus-bicknelli clade and to resolve the phylogeny of the migratory species of Catharus. Our dataset included more than 2,000 loci and over 1,700 variable genotyped sites, and analyses supported our prediction of divergence with gene flow in the fully migratory clade, with significant gene flow among all three species. Our phylogeny of the genus differs from past work in its placement of C. ustulatus, and further analyses suggest historic gene flow throughout the genus, producing genetically reticulate (or network) phylogenies. This raises questions about trait origins and suggests that seasonal migration and the resulting migratory condition of heteropatry is likely to promote hybridization not only during pairwise divergence and speciation, but also among non-sisters.
The loss of hemoglobin and myoglobin does not minimize oxidative stress in Antarctic icefishes
KM O’Brien, EL Crockett, J Philip, CA Oldham, M Hoffman, DE Kuhn, R Barry, J McLaughliN
Abstract:
The unusual pattern of expression of hemoglobin (Hb) and myoglobin (Mb) among Antarctic notothenioid fishes provides an exceptional model system for assessing the impact of these proteins on oxidative stress. We tested the hypothesis that the lack of oxygen-binding proteins may reduce oxidative stress. Levels and activity of pro-oxidants and small-molecule and enzymatic antioxidants, and levels of oxidized lipids and proteins in the liver, oxidative skeletal muscle and heart ventricle were quantified in five species of notothenioid fishes differing in the expression of Hb and Mb. Levels of ubiquitinated proteins and rates of protein degradation by the 20S proteasome were also quantified. Although levels of oxidized proteins and lipids, ubiquitinated proteins, and antioxidants were higher in red-blooded fishes than in Hb-less icefishes in some tissues, this pattern did not persist across all tissues. Expression of Mb was not associated with oxidative damage in the heart ventricle, whereas the activity of citrate synthase and the contents of heme were positively correlated with oxidative damage in most tissues. Despite some tissue differences in levels of protein carbonyls among species, rates of degradation by the 20S proteasome were not markedly different, suggesting either alternative pathways for eliminating oxidized proteins or that redox tone varies among species. Together, our data indicate that the loss of Hb and Mb does not correspond with a clear pattern of either reduced oxidative defense or oxidative damage.
Cold acclimation increases levels of some heat shock protein and sirtuin isoforms in threespine stickleback
LE Teigen, JI Orczewska, J McLaughlin, KM O’Brien
Abstract:
Molecular chaperones [heat shock proteins (HSPs)] increase in response to rapid changes in temperatures, but long-term acclimation to cold temperature may also warrant elevations in HSPs. In fishes, cold acclimation increases mitochondrial density and oxidative stress in some tissues, which may increase demand for HSPs. We hypothesized that levels of HSPs, as well as sirtuins (SIRTs), NAD-dependent deacetylases that mediate changes in metabolism and responses to oxidative stress (including increases in HSPs), would increase during cold acclimation of threespine stickleback (Gasterosteus aculeatus). Transcript levels of hsp70, hsc70, hsp60 and hsp90-α, sirts1–4, as well as protein levels of HSP60, HSP90 and HSC70 were quantified in liver and pectoral adductor muscle of stickleback during cold acclimation from 20 °C to 8 °C. In liver, cold acclimation stimulated a transient increase in mRNA levels of hsp60 and hsc70. Transcript levels of sirt1 and sirt2 also increased in response to cold acclimation and remained elevated. In pectoral muscle, mRNA levels of hsp60, hsp90-α, hsc70 and sirt1 all transiently increased in response to cold acclimation, while levels of sirts2–4 remained constant or declined. Similar to transcript levels, protein levels of HSC70 increased in both liver and pectoral muscle. Levels of HSP90 also increased in liver after 4 weeks at 8 °C. HSP60 remained unchanged in both tissues, as did HSP90 in pectoral muscle. Our results indicate that while both HSPs and SIRTs increase in response to cold acclimation in stickleback, the response is tissue and isoform specific, likely reflecting differences in metabolism and oxidative stress.