Unraveling Adaptive Evolutionary Divergence at Microgeographic Scales.

AbstractStriking examples of local adaptation at fine geographic scales are increasingly being documented in natural populations. However, the relative contributions made by natural selection, phenotype-dependent dispersal (when individuals disperse with respect to a habitat preference), and mate preference in generating and maintaining microgeographic adaptation and divergence are not well studied. Here, we develop quantitative genetics models and individual-based simulations (IBSs) to uncover the evolutionary forces that possibly drive microgeographic divergence. We also perform Bayesian estimation of the parameters in our IBS using empirical data on habitat-specific variation in bill morphology in the island scrub-jay (Aphelocoma insularis) to apply our models to a natural system. We find that natural selection and phenotype-dependent dispersal can generate the patterns of divergence we observe in the island scrub-jay. However, mate preference for a mate with similar bill morphology, even though observed in the species, does not play a significant role in driving divergence. Our modeling approach provides insights into phenotypic evolution occurring over small spatial scales relative to dispersal ranges, suggesting that adaptive divergence at microgeographic scales may be common across a wider range of taxa than previously thought. Our quantitative genetic models help to inform future theoretical and empirical work to determine how selection, habitat preference, and mate preference contribute to local adaptation and microgeographic divergence.

A lack of genetic diversity and minimal adaptive evolutionary divergence in introduced Mysis shrimp after 50 years.

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, F ST 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.

Population genomics indicate three different modes of divergence and speciation with gene flow in the green-winged teal duck complex.

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 âˆ¼0.1-0.4 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.

Habitat-linked genetic variation supports microgeographic adaptive divergence in an island-endemic bird species.

We investigated the potential mechanisms driving habitat-linked genetic divergence within a bird species endemic to a single 250-km2 island. The island scrub-jay (Aphelocoma insularis) exhibits microgeographic divergence in bill morphology across pine-oak ecotones on Santa Cruz Island, California (USA), similar to adaptive differences described in mainland congeners over much larger geographic scales. To test whether individuals exhibit genetic differentiation related to habitat type and divergence in bill length, we genotyped over 3000 single nucleotide polymorphisms in 123 adult island scrub-jay males from across Santa Cruz Island using restriction site-associated DNA sequencing. Neutral landscape genomic analyses revealed that genome-wide genetic differentiation was primarily related to geographic distance and differences in habitat composition. We also found 168 putatively adaptive loci associated with habitat type using multivariate redundancy analysis while controlling for spatial effects. Finally, two genome-wide association analyses revealed a polygenic basis to variation in bill length with multiple loci detected in or near genes known to affect bill morphology in other birds. Our findings support the hypothesis that divergent selection at microgeographic scales can cause adaptive divergence in the presence of ongoing gene flow.

Cardiovascular responses to progressive hypoxia in ducks native to high altitude in the Andes.

The cardiovascular system is critical for delivering O2 to tissues. Here, we examined the cardiovascular responses to progressive hypoxia in four high-altitude Andean duck species compared with four related low-altitude populations in North America, tested at their native altitude. Ducks were exposed to stepwise decreases in inspired partial pressure of O2 while we monitored heart rate, O2 consumption rate, blood O2 saturation, haematocrit (Hct) and blood haemoglobin (Hb) concentration. We calculated O2 pulse (the product of stroke volume and the arterial-venous O2 content difference), blood O2 concentration and heart rate variability. Regardless of altitude, all eight populations maintained O2 consumption rate with minimal change in heart rate or O2 pulse, indicating that O2 consumption was maintained by either a constant arterial-venous O2 content difference (an increase in the relative O2 extracted from arterial blood) or by a combination of changes in stroke volume and the arterial-venous O2 content difference. Three high-altitude taxa (yellow-billed pintails, cinnamon teal and speckled teal) had higher Hct and Hb concentration, increasing the O2 content of arterial blood, and potentially providing a greater reserve for enhancing O2 delivery during hypoxia. Hct and Hb concentration between low- and high-altitude populations of ruddy duck were similar, representing a potential adaptation to diving life. Heart rate variability was generally lower in high-altitude ducks, concurrent with similar or lower heart rates than low-altitude ducks, suggesting a reduction in vagal and sympathetic tone. These unique features of the Andean ducks differ from previous observations in both Andean geese and bar-headed geese, neither of which exhibit significant elevations in Hct or Hb concentration compared with their low-altitude relatives, revealing yet another avian strategy for coping with high altitude.

Cardiovascular responses to progressive hypoxia in ducks native to high altitude in the Andes.

The cardiovascular system is critical for delivering O2 to tissues. Here we examine the cardiovascular responses to progressive hypoxia in four high-altitude Andean duck species compared to four related low-altitude populations in North America, tested at their native altitude. Ducks were exposed to stepwise decreases in inspired partial pressure of O2 while we monitored heart rate, O2 consumption rate, blood O2 saturation, haematocrit (Hct), and blood haemoglobin concentration [Hb]. We calculated O2 pulse (the product of stroke volume and the arterial-venous O2 content difference), blood O2 concentration, and heart rate variability. Regardless of altitude, all eight populations maintained O2 consumption rate with minimal change in heart rate or O2 pulse, indicating that O2 consumption was maintained by either a constant arterial-venous O2 content difference (an increase in the relative O2 extracted from arterial blood) or by a combination of changes in stroke volume and the arterial-venous O2 content difference. Three high-altitude taxa (yellow-billed pintails, cinnamon teal, and speckled teal) had higher Hct and [Hb], increasing the O2 content of arterial blood, and potentially providing a greater reserve for enhancing O2 delivery during hypoxia. Hct and [Hb] between low- and high-altitude populations of ruddy duck were similar, representing a potential adaptation to diving life. Heart rate variability was generally lower in high-altitude ducks, concurrent with similar or lower heart rates than low-altitude ducks, suggesting a reduction in vagal and sympathetic tone. These unique features of the Andean ducks differ from previous observations in both Andean geese and bar-headed geese, neither of which exhibit significant elevations in Hct or [Hb] compared to their low-altitude relatives, revealing yet another avian strategy for coping with high altitude.

Control of breathing and respiratory gas exchange in high-altitude ducks native to the Andes.

We examined the control of breathing and respiratory gas exchange in six species of high-altitude duck that independently colonized the high Andes. We compared ducks from high-altitude populations in Peru (Lake Titicaca at ∼3800 m above sea level; Chancay River at ∼3000-4100 m) with closely related populations or species from low altitude. Hypoxic ventilatory responses were measured shortly after capture at the native altitude. In general, ducks responded to acute hypoxia with robust increases in total ventilation and pulmonary O2 extraction. O2 consumption rates were maintained or increased slightly in acute hypoxia, despite ∼1-2°C reductions in body temperature in most species. Two high-altitude taxa - yellow-billed pintail and torrent duck - exhibited higher total ventilation than their low-altitude counterparts, and yellow-billed pintail exhibited greater increases in pulmonary O2 extraction in severe hypoxia. In contrast, three other high-altitude taxa - Andean ruddy duck, Andean cinnamon teal and speckled teal - had similar or slightly reduced total ventilation and pulmonary O2 extraction compared with low-altitude relatives. Arterial O2 saturation (SaO2 ) was elevated in yellow-billed pintails at moderate levels of hypoxia, but there were no differences in SaO2  in other high-altitude taxa compared with their close relatives. This finding suggests that improvements in SaO2  in hypoxia can require increases in both breathing and haemoglobin-O2 affinity, because the yellow-billed pintail was the only high-altitude duck with concurrent increases in both traits compared with its low-altitude relative. Overall, our results suggest that distinct physiological strategies for coping with hypoxia can exist across different high-altitude lineages, even among those inhabiting very similar high-altitude habitats.

Respiratory mechanics of eleven avian species resident at high and low altitude.

The metabolic cost of breathing at rest has never been successfully measured in birds, but has been hypothesized to be higher than in mammals of a similar size because of the rocking motion of the avian sternum being encumbered by the pectoral flight muscles. To measure the cost and work of breathing, and to investigate whether species resident at high altitude exhibit morphological or mechanical changes that alter the work of breathing, we studied 11 species of waterfowl: five from high altitudes (>3000 m) in Perú, and six from low altitudes in Oregon, USA. Birds were anesthetized and mechanically ventilated in sternal recumbency with known tidal volumes and breathing frequencies. The work done by the ventilator was measured, and these values were applied to the combinations of tidal volumes and breathing frequencies used by the birds to breathe at rest. We found the respiratory system of high-altitude species to be of a similar size, but consistently more compliant than that of low-altitude sister taxa, although this did not translate to a significantly reduced work of breathing. The metabolic cost of breathing was estimated to be between 1 and 3% of basal metabolic rate, as low or lower than estimates for other groups of tetrapods.

Mitochondrial physiology in the skeletal and cardiac muscles is altered in torrent ducks, Merganetta armata, from high altitudes in the Andes.

Torrent ducks inhabit fast-flowing rivers in the Andes from sea level to altitudes up to 4500 m. We examined the mitochondrial physiology that facilitates performance over this altitudinal cline by comparing the respiratory capacities of permeabilized fibers, the activities of 16 key metabolic enzymes and the myoglobin content in muscles between high- and low-altitude populations of this species. Mitochondrial respiratory capacities (assessed using substrates of mitochondrial complexes I, II and/or IV) were higher in highland ducks in the gastrocnemius muscle - the primary muscle used to support swimming and diving - but were similar between populations in the pectoralis muscle and the left ventricle. The heightened respiratory capacity in the gastrocnemius of highland ducks was associated with elevated activities of cytochrome oxidase, phosphofructokinase, pyruvate kinase and malate dehydrogenase (MDH). Although respiratory capacities were similar between populations in the other muscles, highland ducks had elevated activities of ATP synthase, lactate dehydrogenase, MDH, hydroxyacyl CoA dehydrogenase and creatine kinase in the left ventricle, and elevated MDH activity and myoglobin content in the pectoralis. Thus, although there was a significant increase in the oxidative capacity of the gastrocnemius in highland ducks, which correlates with improved performance at high altitudes, the variation in metabolic enzyme activities in other muscles not correlated to respiratory capacity, such as the consistent upregulation of MDH activity, may serve other functions that contribute to success at high altitudes.