Panamanian Populations Research Articles

Dynamics of Mask Use as a Prevention Strategy against SARS-CoV-2 in Panama

Early in the SARS-CoV-2 pandemic, many national public health authorities implemented non-pharmaceutical interventions to mitigate disease outbreaks. Panamá established mandatory mask use two months after its first documented case. Initial compliance was high, but diverse masks were used in public areas. We studied behavioral dynamics of mask use through the first two COVID-19 waves in Panama, to improve the implementation of effective, low-cost public health containment measures when populations are exposed to novel air-borne pathogens. Mask use behavior was recorded from pedestrians in four Panamanian populations (August to December 2020). We recorded facial coverings and if used, the type of mask, and gender and estimated age of the wearer. Our results showed that people were highly compliant (>95%) with mask mandates and demonstrated important population-level behaviors: (1) decreasing use of cloth masks over time, and increasing use of surgical masks; (2) mask use was 3-fold lower in suburban neighborhoods than other public areas and (3) young people were least likely to wear masks. Results help focus on highly effective, low-cost, public health interventions for managing and controlling a pandemic. Considerations of behavioral preferences for different masks, relative to pricing and availability, are essential for optimizing public health policies. Policies to increase the availability of effective masks, and behavioral nudges to increase acceptance, and to facilitate mask usage, during the ongoing SARS-CoV-2 pandemic, and for future pandemics of respiratory pathogens, are key tools, especially for nations lagging in access to expensive vaccines and pharmacological approaches.

Inheritance, distribution and genetic differentiation of a color polymorphism in Panamanian populations of the tortoise beetle, Chelymorpha alternans (Coleoptera: Chrysomelidae).

Intraspecific variation maintained in natural populations has long intrigued scientists and naturalists. One form of this variation, color polymorphisms, provide a rich opportunity to connect genotypic and phenotypic diversity within an ecological and evolutionary context. The existence of color polymorphisms in Panamanian populations of the Neotropical tortoise beetle, Chelymorpha alternans, has been suspected but never systematically explored. To characterize geographic distribution and underlying genetics we sampled a total of 3819 beetles from 28 sites across Panama, quantifying five distinct phenotypes. Two phenotypes, the "metallic" and "rufipennis" are the most widely distributed phenotypes, occurring in nearly all collecting sites. The "veraguensis" phenotype was found to be restricted to the Western end of the Isthmus and the "militaris" phenotypes restricted to sites east of the canal. Controlled matings between phenotypes and reared offspring revealed no indications of reproductive barriers, even among phenotypes which do not co-occur in nature. Color pattern phenotype is largely controlled by Mendelian assortment of four alleles competing at a single locus. A clear dominance hierarchy exists among alleles, with two being co-dominant. Genomic scans from 32 individuals revealed low levels of genetic differentiation, with a small fraction of the genome showing a high degree of divergence. The easily observed variation among populations, simple genetic architecture, and rearing capabilities, make this a promising system for investigating proximate and ultimate factors of phenotypic variation.

Highly contrasted population genetic structures in a host-parasite pair in the Caribbean Sea.

Evolution and population genetic structure of marine species across the Caribbean Sea are shaped by two complex factors: the geological history and the present pattern of marine currents. Characterizing and comparing the genetic structures of codistributed species, such as host–parasite associations, allow discriminating the relative importance of environmental factors and life history traits that influenced gene flow and demographic events. Using microsatellite and Cytochrome Oxidase I markers, we investigated if a host–parasite pair (the heart urchin Meoma ventricosa and its parasitic pea crab Dissodactylus primitivus) exhibits comparable population genetic structures in the Caribbean Sea and how the observed patterns match connectivity regions from predictive models and other taxa. Highly contrasting patterns were found: the host showed genetic homogeneity across the whole studied area, whereas the parasite displayed significant differentiation at regional and local scales. The genetic diversity of the parasitic crabs (both in microsatellites and COI) was distributed in two main groups, Panama–Jamaica–St Croix on the one hand, and the South‐Eastern Caribbean on the other. At a smaller geographical scale, Panamanian and Jamaican parasite populations were genetically more similar, while more genetic differentiation was found within the Lesser Antilles. Both species showed a signature of population expansion during the Quaternary. Some results match predictive models or data from previous studies (e.g., the Western‐Eastern dichotomy in the parasite) while others do not (e.g., genetic differentiation within the Lesser Antilles). The sharp dissimilarity of genetic structure of these codistributed species outlines the importance of population expansion events and/or contrasted patterns of gene flow. This might be linked to differences in several life history traits such as fecundity (higher for the host), swimming capacity of larval stages (higher for the parasite), and habitat availability (higher for the host).

No evidence for maintenance of a sympatric Heliconius species barrier by chromosomal inversions.

Mechanisms that suppress recombination are known to help maintain species barriers by preventing the breakup of coadapted gene combinations. The sympatric butterfly species Heliconius melpomene and Heliconius cydno are separated by many strong barriers, but the species still hybridize infrequently in the wild, and around 40% of the genome is influenced by introgression. We tested the hypothesis that genetic barriers between the species are maintained by inversions or other mechanisms that reduce between‐species recombination rate. We constructed fine‐scale recombination maps for Panamanian populations of both species and their hybrids to directly measure recombination rate within and between species, and generated long sequence reads to detect inversions. We find no evidence for a systematic reduction in recombination rates in F1 hybrids, and also no evidence for inversions longer than 50 kb that might be involved in generating or maintaining species barriers. This suggests that mechanisms leading to global or local reduction in recombination do not play a significant role in the maintenance of species barriers between H. melpomene and H. cydno.

ORIGINS AND GENETIC DIVERSITY OF INTRODUCED POPULATIONS OF THE PUERTO RICAN RED-EYED COQUÍ, ELEUTHERODACTYLUS ANTILLENSIS, IN SAINT CROIX (U.S. VIRGIN ISLANDS) AND PANAMÁ.

The Red-eyed Coquí, Eleutherodactylus antillensis, is a terrestrial frog endemic to the Puerto Rican Bank (Puerto Rico and numerous islands and cays off its eastern coast), in the eastern Caribbean Sea. The species was likely introduced in Saint Croix, an island c. 100 km southeast of Puerto Rico, in the late 1930s, and in Panamá City, Panamá, in the late 1950s or early 1960s, but the source(s) of these introductions are unknown. We analyzed sequence data from one mtDNA locus and four nuDNA introns to infer the origin(s) of the Saint Croix and Panamá City populations and quantify their genetic diversity. Saint Croix and Panamanian populations do not share any haplotypes, and they cluster with different native populations, suggesting that they are derived from separate sources in the Puerto Rican Bank. Patterns of population structure trace the probable sources of E. antillensis in Saint Croix to islands off Puerto Rico's eastern coast, which include Vieques, Culebra, Saint Thomas, Saint John, Tortola, and Virgin Gorda, and possibly to eastern Puerto Rico as well. In contrast, Panamá City E. antillensis probably originated from either western or eastern Puerto Rico. Genetic diversity in the introduced populations is similar to or lower than in populations in the species' native range, indicating that genetic diversity has not increased in the alien frogs. Our findings may facilitate the development of preventive measures to minimize introductions of non-native amphibians in the Caribbean and Central America.

Major histocompatibility complex selection dynamics in pathogen-infected túngara frog (Physalaemus pustulosus) populations.

Pathogen-driven selection can favour major histocompatibility complex (MHC) alleles that confer immunological resistance to specific diseases. However, strong directional selection should deplete genetic variation necessary for robust immune function in the absence of balancing selection or challenges presented by other pathogens. We examined selection dynamics at one MHC class II (MHC-II) locus across Panamanian populations of the túngara frog, Physalaemus pustulosus, infected by the amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd). We compared MHC-II diversity in highland túngara frog populations, where amphibian communities have experienced declines owing to Bd, with those in the lowland region that have shown no evidence of decline. Highland region frogs had MHC variants that confer resistance to Bd. Variant fixation appeared to occur by directional selection rather than inbreeding, as overall genetic variation persisted in populations. In Bd-infected lowland sites, however, selective advantage may accrue to individuals with only one Bd-resistance allele, which were more frequent. Environmental conditions in lowlands should be less favourable for Bd infection, which may reduce selection for specific Bd resistance in hosts. Our results suggest that MHC selection dynamics fluctuate in túngara frog populations as a function of the favourability of habitat to pathogen spread and the vulnerability of hosts to infection.

Revisiting the Diego Blood Group System in Amerindians: Evidence for Gene-Culture Comigration.

Six decades ago the DI*A allele of the Diego blood group system was instrumental in proving Native American populations originated from Siberia. Since then, it has received scant attention. The present study was undertaken to reappraise distribution of the DI*A allele in 144 Native American populations based on current knowledge. Using analysis of variance tests, frequency distribution was studied according to geographical, environmental, and cultural parameters. Frequencies were highest in Amazonian populations. In contrast, DI*A was undetectable in subarctic, Fuegian, Panamanian, Chaco and Yanomama populations. Closer study revealed a correlation that this unequal distribution was correlated with language, suggesting that linguistic divergence was a driving force in the expansion of DI*A among Native Americans. The absence of DI*A in circumpolar Eskimo-Aleut and Na-Dene speakers was consistent with a late migratory event confined to North America. Distribution of DI*A in subtropical areas indicated that gene and culture exchanges were more intense within than between ecozones. Bolstering the utility of classical genetic markers in biological anthropology, the present study of the expansion of Diego blood group genetic polymorphism in Native Americans shows strong evidence of gene-culture comigration.

Systematics of the Rhinellamargaritifera complex (Anura, Bufonidae) from western Ecuador and Panama with insights in the biogeography of Rhinellaalata.

The Rhinella margaritifera species group consists of 17 species of toads distributed in tropical and subtropical South America and eastern Central America. The identity of some of its species is poorly understood and there are numerous undescribed cryptic species. Among them, the status of Rhinella margaritifera is one of the most problematic. Its range includes lowland rainforests separated by the Andes, the Chocoan rainforest to the west and the Amazonian rainforest to the east. This distribution is puzzling because the Andes are an old and formidable barrier to gene flow and therefore should generate vicariant speciation between disjunct lowland populations. Herein we clarify the taxonomy of populations of the Rhinella margaritifera complex from Central America and the Chocó region of South America. The morphological and genetic variation of Rhinella margaritifera was examined from 39 populations from Chocó, 24 from the upper Amazon region of Ecuador, and 37 from Panama, including the holotype of the Panamanian Rhinella alata. Phylogenetic analyses were performed based on mitochondrial genes 12S rRNA, 16S rRNA, and cytochrome c oxidase I (COI) and the nuclear gene Tyrosinase (Tyr). The genetic and morphological data show that Panamanian and Chocoan populations are conspecific. In the phylogeny, populations from Chocó and Panama form a well-supported clade. The morphology of the holotype of Rhinella alata falls within the variation range of Panamanian and Chocoan populations. Based on all this evidence, we assign the populations from western Ecuador and Panama to Rhinella alata and demonstrate that the unusual distribution pattern of “Rhinella margaritifera” on both sides of the Andes was an artifact of incorrectly defined species boundaries.

Sisters' curse: sexually antagonistic effects constrain the spread of a mitochondrial haplogroup superior in sperm competition.

Maternal inheritance of mitochondria creates a sex-specific selective sieve with implications for male longevity, disease susceptibility and infertility. Because males are an evolutionary dead end for mitochondria, mitochondrial mutations that are harmful or beneficial to males but not females cannot respond directly to selection. Although the importance of this male/female asymmetry in evolutionary response depends on the extent to which mitochondrial mutations exert antagonistic effects on male and female fitness, few studies have documented sex-specific selection acting on mitochondria. Here, we exploited the discovery of two highly divergent mitochondrial haplogroups (A and B2) in central Panamanian populations of the pseudoscorpion Cordylochernes scorpioides. Next-generation sequencing and phylogenetic analyses suggest that selection on the ND4 and ND4L mitochondrial genes may partially explain sexually antagonistic mitochondrial effects on reproduction. Males carrying the rare B2 mitochondrial haplogroup enjoy a marked advantage in sperm competition, but B2 females are significantly less sexually receptive at second mating than A females. This reduced propensity for polyandry is likely to significantly reduce female lifetime reproductive success, thereby limiting the spread of the male beneficial B2 haplogroup. Our findings suggest that maternal inheritance of mitochondria and sexually antagonistic selection can constrain male adaptation and sexual selection in nature.

Jumping a geographic barrier: diversification of the mangrove species Pelliciera rhizophorae (Tetrameristaceae) across the Central American Isthmus

The Central American Isthmus (CAI) is an important geographic barrier in the Neotropics. Its role in the diversification of marine and coastal species has been detected in fishes, turtles, sea urchins, and mangroves. We evaluated the CAI’s influence on the diversification of the most ancient neotropical mangrove species Pelliciera rhizophorae across populations from the Caribbean and Pacific coasts, based on the analysis of ten nuclear microsatellite loci and two noncoding chloroplast DNA regions. The two molecular markers showed concordant patterns of diversification in this mangrove species. Contrary to our expectations, this study did not reveal significant genetic structure among populations separated by the CAI. Two major genetic variants (cluster I and cluster II) were found on both coasts, but the two were not found intermixed in the same population. Within each coastal region, breaking of gene flow among populations was found at two points in the Pacific Basin and one point in the Caribbean Basin, separating the Colombian and Panamanian populations. Our study revealed a transisthmian connection among populations of P. rhizophorae. This result, together with the reduced genetic diversity in the Caribbean reported in our previous study, suggests the recent origin of these populations, probably due to reintroduction of P. rhizophorae from the Pacific coast. Taking into account that these introductions are random events, this study raises a new question: Why are genetic variants not intermixed within the Caribbean populations? Our hypotheses suggest the influence of environmental factors and/or anthropogenic impact on the establishment of these Caribbean patches.

Relaciones entre los bovinos criollos panameños y algunas razas criollas de Latinoamérica

El objetivo de este trabajo fue establecer la relación genética entre poblaciones bovinas panameñas Guabalá y Guaymí y algunas poblaciones criollas de Latinoamérica. Se practicó un análisis factorial de correspondencias, análisis de varianza molecular, distancias genéticas, número medio de migrantes por población y los estadísticos F de Wright. Se evaluó la estructura de la población mediante un modelo Bayesiano, suponiéndose un número desconocido de K grupos diferentes genéticamente. El análisis factorial de correspondencias mostró que las poblaciones Guabalá y Guaymí se agrupan con los bovinos criollos mexicanos y el Texas Longhorn. Igualmente se observó menor diferenciación genética de las criollas panameñas con mexicanos y el Texas Longhorn. Los análisis de distancia genética también mostraron dados similares a los obtenidos por el Amova y por el análisis factorial de correspondencia, y se observó menor distancia entre poblaciones del norte y las panameñas, en comparación con las poblaciones del sur. La agrupación bayesiana permitió la asignación de los individuos a su respectivo grupo, con base en su semejanza genética, y proporcionó información acerca del número de poblaciones bajo el cual se originan. Hay una estrecha relación histórica, genética y geográfica de las poblaciones panameñas, criollas mexicanas y Texas Longhorn, a partir de las migraciones de sus precursores desde las Antillas hacia Panamá y México.

A chocolate a day keeps the doctor away?

A chocolate a day keeps the doctor away?

Genetic and phenotypic variation in a colourful treefrog across five geographic barriers

Aim Understanding the patterns and processes underlying phenotype in a polytypic species provides key insights into microevolutionary mechanisms of diversification. The red-eyed treefrog, Agalychnis callidryas, exhibits strong regional differentiation in colour pattern, corresponding to five admixed mitochondrial DNA clades. We evaluated spatial diversity patterns across multiple, putative barriers to examine the fine-scale processes that mediate phenotypic divergence between some regions while maintaining homogeneity between others. Location We examined patterns of phenotypic diversification among 17 sites that span five putative biogeographic barriers in lower Central America (Costa Rica and Panama). Methods We tested the extent to which genetic distance (FST) derived from six multilocus nuclear genotypes covaried with measures of phenotypic distance (leg coloration) within and between biogeographic regions. We used linear regression analyses to determine the role of geographic and genetic factors in structuring spatial patterns of phenotypic diversity. Results The factors that best explained patterns of phenotypic diversity varied among biogeographic regions. We identified one geographic barrier that impeded gene exchange and resulted in concordant phenotypic divergence across the Continental Divide, isolating Caribbean and Pacific populations. Across Caribbean Costa Rican populations, one barrier structured phenotypic but not genetic diversity patterns, indicating a role for selection. In other regions, the putative barriers had no determining effect on either genetic or leg colour structure. Main conclusions The processes mediating the distribution and diversification of colour pattern in this polytypic, wide-ranging treefrog varied among biogeographic regions. Spatially varying selection combined with the isolating effects of geographic factors probably resulted in the patchy distribution of colour diversity across Costa Rican and Panamanian populations.

Collection and characterization of maize and upland rice populations cropped by poor farmers in the uplands of Panama's Azuero region

The conservation of crop genetic resources is an international priority and requires the continued collection and characterization of farmer varieties. We collected and characterized maize and upland rice populations cropped by farmers in Panama's Azuero region. The objective of our study was to evaluate the crop genetic diversity of farmer varieties of maize and upland rice grown by poor farmers in Panama. We found that: (1) farmers' naming practices only partially corresponded to genetic relationships and were the strongest for rice populations; (2) farmers' classification of populations as ‘modern’ or ‘traditional’ was reflected in phenotypic differences; (3) Panamanian maize populations were molecularly distinct from populations collected elsewhere in Latin America; and (4) heterogeneous rice populations were common and heterogeneity was often due to admixture of recognized farmer varieties. Our results indicate that poor farmers in Panama continue to farm ‘traditional’ varieties that harbour genetic diversity of interest. There has, however, been substantial adoption of ‘modern’ varieties.

Y-Chromosome Variability in Four Native American Populations from Panama

The allele and haplotype frequencies for 13 Y-chromosome short tandem repeats (STRs) [nine STR loci of the minimal Y-chromosome haplotype (DYS19 -DYS385a -DYS385b -DYS389I -DYS389II -DYS390 -DYS391 - DYS392 -DYS393) plus four additional loci (DYS388, DYS426, DYS439, DXYS156)] were determined in 99 males from 4 Panamanian native American populations, including the Chibcha-speaking Ngöbé and Kuna and the Chocóspeaking Emberá and Wounan. Fifty haplotypes were identified, of which 48 (96%) were specific to a single population and 29 (63%) were found in only a single individual. Gene diversity per locus per population ranged from 0 to 0.814, with the highest gene diversity present at the DYS389II locus in the Emberá. The haplotypic discrimination capacity was low, ranging from 42.3% in the Kuna to 63.1% in theWounan. The four tribes showed a high degree of differentiation both at the Y chromosome and in the mitochondrial genome, highlighting the importance of genetic structure even in geographically proximate and linguistically related populations.

Y-Chromosome Variability in Four Native American Populations from Panama

The allele and haplotype frequencies for 13 Y-chromosome short tandem repeats (STRs) [nine STR loci of the minimal Y-chromosome haplotype (DYS19 - DYS385a - DYS385b - DYS389I - DYS389II - DYS390 - DYS391- DYS392 - DYS393) plus four additional loci (DYS388, DYS426, DYS439, DXYS156)] were determined in 99 males from 4 Panamanian native American populations, including the Chibcha-speaking Ngöbé and Kuna and the Chocó-speaking Emberá and Wounan. Fifty haplotypes were identified, of which 48 (96%) were specific to a single population and 29 (63%) were found in only a single individual. Gene diversity per locus per population ranged from 0 to 0.814, with the highest gene diversity present at the DYS389II locus in the Emberá. The haplotypic discrimination capacity was low, ranging from 42.3% in the Kuna to 63.1% in the Wounan. The four tribes showed a high degree of differentiation both at the Y chromosome and in the mitochondrial genome, highlighting the importance of genetic structure even in geographically proximate and linguistically related populations.

Geographic Variation in Male Sexual Signals in Strawberry Poison Frogs (Dendrobates pumilio)

AbstractIn this paper, we compare the advertisement calls of 207 neotropical strawberry poison frogs (Dendrobates pumilio) collected in 21 localities along a transect from northern Costa Rica to western Panama. Populations varied most in call duration and call rate, while pulse rate and duty cycle were less variable. Multivariate analyses showed that call variation followed a cline with higher call rates, shorter calls, lower duty cycles and higher pulse rates in the southeast. Body size decreased towards the southeast and explained most variation in dominant frequency, as well as some residual variation in call rate. We conclude that a combination of geography and morphology is largely responsible for call variation within this species. Two inferred bio‐acoustic groups were roughly in accordance with two genetic groups, geographically separated in central Costa Rica. However, genetic distances among populations did not co‐vary with call dissimilarity after correction for geographic distances. Thus, differences in calls between genetic groups are probably mainly a result of clinal variation. These findings agree with the general observation that bio‐acoustic variation is often not (highly) associated with genetic divergence. Moreover, colour polymorphism observed among Panamanian populations was not reflected in a higher variability in call parameters relative to the monomorphic Costa Rican populations.

Geographical subdivision, demographic history and gene flow in two sympatric species of intertidal snails, Nerita scabricosta and Nerita funiculata, from the tropical eastern Pacific

The patchy distribution of rocky intertidal communities in the tropical eastern Pacific (TEP) may impose severe constraints on the genetic connectivity among populations of marine invertebrates associated with this habitat. In this study, we analyzed a portion of the mitochondrial cytochrome c oxidase subunit I (COI) gene in two sympatric species of marine snails, Nerita scabricosta and Nerita funiculata, common inhabitants of the rocky intertidal from the Gulf of California (Sea of Cortez) and outer Pacific coast of the southern Baja California (Baja) peninsula to northern South America, to assess genetic connectivity among populations of each species. One of our aims was to determine whether the morphological, behavioral, and ecological differences observed among populations of both species throughout their range in the TEP corresponded to population genetic differences. In addition, we were interested in elucidating the demographic history of both species. We found no evidence of genetic structure throughout the Gulf of California and outer coast of the Baja peninsula region for either species. Comparisons between Gulf of California/Baja and Panama populations, however, showed significant genetic differentiation for N. scabricosta, but not for N. funiculata. The genetic differences between Mexican and Panamanian populations of N. scabricosta were consistent with previously reported ecological and behavioral differences for this species between these two distant regions. However, previously reported size differences between northern and central/southern Gulf of California individuals of N. scabricosta do not correspond with our findings of genetic connectivity among these populations. Results from neutrality tests (Tajima’s D and Fu’s FS), the mismatch distribution, and Bayesian skyline analyses suggested that both species have experienced dramatic population expansions dating to the Pleistocene.

Female Associative Behavior Accompanies Morphological Distinction in Two Panamanian Populations of the Molly Poecilia gilli (Kner)

ABSTRACT We investigated the associative behavior of the female molly (Pisces: Poeciliidae), Poecilia gilli (Kner), collected from two Panamanian populations—one from a clear running forest stream and the other from an impacted suburban stream. We tested the hypotheses that females would preferentially associate with males and females of their local population versus the foreign population and that males would prefer local females. We also tested the hypothesis that morphological distinctions between the two populations can be made. We found that females preferentially associated with local males but preferred neither local nor foreign females. Males exhibited no preference for females based on stream of origin. Dorsal fin height differed between populations but sex had no effect on this trait. Ecological factors or female preference could be responsible for this divergence, which could be reinforced by female preference for local males.

Genetic variability and population structure among wild Baird's tapirs

AbstractBaird's tapir, Tapirus bairdii, is an endangered, large, Central American mammal whose shy behaviour, solitary social structure and preference for deep tropical forests make it difficult to study using traditional field biology techniques. Despite great concern regarding its conservation status, very little is known about its population structure, mating system or dispersal patterns, information needed for designing appropriate management plans. Molecular genetic approaches can be of use in obtaining such information. In this study, we developed six polymorphic microsatellite genetic markers from genomic libraries of T. bairdii and T. terrestris. Using these markers, we completed the first assessment of genetic variability and population genetic structure in Baird's tapirs. Populations from southern Costa Rica and southern Panama were found to have low levels of genetic variability (allelic content, heterozygosity) but no indication of a recent population bottleneck. Bayesian and standard (F‐statistic) analyses of genotype data indicate that the southern Costa Rican and southern Panamanian populations of Baird's tapirs were connected by some (at least one migrant per generation) gene flow prior to the destruction of intermittent habitat. These results indicate that the connection of these two populations by a MesoAmerican Biological Corridor (MBC) would be appropriate.