Luis Fernando De León

Reproductive isolation of sympatric morphs in a population of Darwin's finches

Recent research on speciation has identified a central role for ecological divergence, which can initiate speciation when (i) subsets of a species or population evolve to specialize on different ecological resources and (ii) the resulting phenotypic modes become reproductively isolated. Empirical evidence for these two processes working in conjunction, particularly during the early stages of divergence, has been limited. We recently described a population of the medium ground finch, Geospiza fortis, that features large and small beak morphs with relatively few intermediates. As in other Darwins finches of the Galápagos Islands, these morphs presumably diverged in response to variation in local food availability and inter- or intraspecific competition. We here demonstrate that the two morphs show strong positive assortative pairing, a pattern that holds over three breeding seasons and during both dry and wet conditions. We also document restrictions on gene flow between the morphs, as revealed by genetic variation at 10 microsatellite loci. Our results provide strong support for the central role of ecology during the early stages of adaptive radiation.

Disruptive selection in a bimodal population of Darwin's finches.

A key part of the ecological theory of adaptive radiation is disruptive selection during periods of sympatry. Some insight into this process might be gained by studying populations that are bimodal for dual-context traits, i.e. those showing adaptive divergence and also contributing to reproductive isolation. A population meeting these criteria is the medium ground finch (Geospiza fortis) of El Garrapatero, Santa Cruz Island, Galápagos. We examined patterns of selection in this population by relating individual beak sizes to interannual recaptures during a prolonged drought. Supporting the theory, disruptive selection was strong between the two beak size modes. We also found some evidence of selection against individuals with the largest and smallest beak sizes, perhaps owing to competition with other species or to gaps in the underlying resource distribution. Selection may thus simultaneously maintain the current bimodality while also constraining further divergence. Spatial and temporal variation in G. fortis bimodality suggests a dynamic tug of war among factors such as selection and assortative mating, which may alternatively promote or constrain divergence during adaptive radiation.

Divergence with gene flow as facilitated by ecological differences: within-island variation in Darwin's finches

Divergence and speciation can sometimes proceed in the face of, and even be enhanced by, ongoing gene flow. We here study divergence with gene flow in Darwins finches, focusing on the role of ecological/adaptive differences in maintaining/promoting divergence and reproductive isolation. To this end, we survey allelic variation at 10 microsatellite loci for 989 medium ground finches (Geospiza fortis) on Santa Cruz Island, Galápagos. We find only small genetic differences among G. fortis from different sites. We instead find noteworthy genetic differences associated with beak. Moreover, G. fortis at the site with the greatest divergence in beak size also showed the greatest divergence at neutral markers; i.e. the lowest gene flow. Finally, morphological and genetic differentiation between the G. fortis beak-size morphs was intermediate to that between G. fortis and its smaller (Geospiza fuliginosa) and larger (Geospiza magnirostris) congeners. We conclude that ecological differences associated with beak size (i.e. foraging) influence patterns of gene flow within G. fortis on a single island, providing additional support for ecological speciation in the face of gene flow. Patterns of genetic similarity within and between species also suggest that interspecific hybridization might contribute to the formation of beak-size morphs within G. fortis.

EXPLORING POSSIBLE HUMAN INFLUENCES ON THE EVOLUTION OF DARWIN'S FINCHES

Humans are an increasingly common influence on the evolution of natural populations. Potential arenas of influence include altered evolutionary trajectories within populations and modifications of the process of divergence among populations. We consider this second arena in the medium ground finch (Geospiza fortis) on Santa Cruz Island, Galápagos, Ecuador. Our study compared the G. fortis population at a relatively undisturbed site, El Garrapatero, to the population at a severely disturbed site, Academy Bay, which is immediately adjacent to the town of Puerto Ayora. The El Garrapatero population currently shows beak size bimodality that is tied to assortative mating and disruptive selection, whereas the Academy Bay population was historically bimodal but has lost this property in conjunction with a dramatic increase in local human population density. We here evaluate potential ecological‐adaptive drivers of the differences in modality by quantifying relationships between morphology (beak and head dimensions), functional performance (bite force), and environmental characteristics (diet). Our main finding is that associations among these variables are generally weaker at Academy Bay than at El Garrapatero, possibly because novel foods are used at the former site irrespective of individual morphology and performance. These results are consistent with the hypothesis that the rugged adaptive landscapes promoting and maintaining diversification in nature can be smoothed by human activities, thus hindering ongoing adaptive radiation.

Magic traits: distinguishing the important from the trivial

Servedio et al. [1], following Gavrilets [2], define a magictrait as ‘a trait subject to divergent selection and a traitcontributing to non-random mating that are pleiotropicexpressions of the same gene(s)’. This clarified definition iscertainly helpful, but we outline here several pivotal ques-tions for empirical research, particularly surrounding thecrucial concept of effect size.The effect size of a magic trait, defined by Servedio et al.[1] as ‘how much the trait contributed to the evolution ofincreased reproductive isolation’, determines whether amagic trait is actually important for speciation (an ‘impor-tant magic trait’)or isa ‘trivial magic trait’ (a magic trait ofvery small or zero effect size). Effect size is therefore whatmattersempirically,and yet it isabsent from thedefinitionof a magic trait, which instead embodies theoretical pre-occupations with the genetics underlying traits. We do notpropose to redefine ‘magic trait’, but instead hope to illus-trate how empirical advances will require an explicit focuson effect size. Problematically, however, the definition ofeffect size is retrospective and not generally measurable;empiricalproxiesforeffectsizethatcanbeusedpredictivelyare therefore needed. We here treat the strengths of diver-gentselection, assortativematingand pleiotropy (thethreecomponents of the magic trait definition) as the a prioriexpected contributors to effect size during speciation.Divergent (including disruptive) selection, the first pil-lar of the magic trait definition, is certainly important forspeciation;however,itsmagnitudeismoreimportantthanits mere presence [3]. Moreover, distinguishing weaklydivergent selection from the absence of selection is empiri-cally difficult [4], making it hard to determine whether atrait is magic or non-magic. Fortunately, this distinction isprobablynotofkeyimportancetotheprocessofspeciation,because magic traits under such weak selection are proba-bly trivial. The empirical focus should be on magic traitsexpected to be of large effect size.In addition, spatial and temporal variation in selection[5] makes it difficult to determine whether a trait is gener-allyunderdivergentselection.Forexample,beaksizeintheMedium Ground Finch (Geospiza fortis) has been proposedto be magic [1,6], but selection on beak size is, at varioustimes and places,directional,stabilizing, ordivergent [7,8].Consequently, it is hard to say whether beak size wouldsatisfy the definition; as the selective regime changes, beaksizeswitchesfrommagictonon-magicandbackagain.Thisimpliesthatsuchatraitis,inasense,anordinarytraitthatcontributestonon-randommating,butthatis,attimes,ina‘magic environment’ that subjects it to divergent selection;the magic comes from the trait–environment interaction.Thus, a crucial question emerges: how consistently diver-gent,throughtimeandacrossspace,mustselectionbeforatrait to be magic and also important for speciation? Again,we argue that expected effect size is the key: divergentselection must be sufficiently strong and consistent toactu-ally drive divergence.The second pillar of the definition is non-random mat-ing. However, it is also difficult to distinguish weakly non-randommating fromrandom mating(e.g. [9]), aswell astodetermine the specific trait underlying non-random mat-ing [1]. Moreover, just as with divergent selection, non-randommatingcanvaryinspaceandtime[10].Thus,allofthe difficulties raised above concerning divergent selectionapply with equal strength to non-random mating.The arch connecting these two definitional pillars ispleiotropy; if, instead, the two pillars are influenced by atightly linked pair of genes, that locus is considered only amagic trait ‘mimic’ [1]. Again, empirically differentiatingbetween these two cases is quite difficult [11]. Further-more, the distinction might be of little consequence to thedynamics of speciation; a mimic might have an effect sizejust as large as, or larger than, that of a magic trait [3].Instead, what probably matters is the strength of pleiotro-py or linkage.In summary, empirically distinguishing trivial magictraits from non-magic traits, and magic traits from mimictraits, will prove very difficult. Fortunately, these distinc-tions are largely irrelevant to many questions surroundingspeciation in nature. Instead, the important (although lessprecise) distinction is between traits expected to be of largeeffectsize(whethermagicormimic)versusthoseexpectedtobe of small effect size (whether trivial or non-magic). Tobridge the gap between theoretical and empirical perspec-tives on magic traits, we suggest an increased focus onprobableproxiesforultimateeffectsize,ontheenvironmen-talandecologicalfactorsthatarelikelytobecontributingtoeffect size, and on the evolutionary forces expected to altereffect size through time. With these priorities, a betterunderstanding of the magic of speciation can be expected.

Complete mitochondrial genomes of the New World jacanas: Jacana spinosa and Jacana jacana

Abstract The New World jacanas, Jacana spinosa (Mexico to Panama and also the West Indies) and Jacana jacana (Panama and South America), are polyandrous freshwater waders that are common throughout the Neotropics. These two species hybridize narrowly at their contact zone in Panama, and as part of a study of the hybrid zone dynamics, we present complete, annotated mitochondrial genomes for both species. The two species have very similar mitochondrial genomes, showing identical gene orders, and differing in size in only two RNA features and the control region, and among protein-coding genes, the two genomes had average uncorrected pairwise divergence of 1.8%, ranging from 0.7% for ND4L and 3.6% for ATP8. However, control region divergence is high (∼16%). These mitochondrial genome sequences may be useful tools for understanding jacana hybridization dynamics, especially regarding potential mitonuclear incompatibilities.

Extreme sequence divergence between mitochondrial genomes of two subspecies of White-breasted Wood-wren (Henicorhina leucosticta, Cabanis, 1847) from western and central Panamá

Abstract Prior studies of mitochondrial variation in White-breasted Wood-Wrens (Henicorhina leucosticta) have suggested that populations in South American and Mesoamerica might represent multiple species. Here we report the complete mitochondrial genomes from two individuals of H. leucosticta, representing the Panamanian subspecies pittieri and alexandri. The two sequences were 16,721 and 16,726 base pairs in size with both genomes comprised of the usual 22 tRNA genes, 2 rRNA genes, 13 protein-coding genes, and one displacement loop region in the standard avian order. Uncorrected pairwise divergence between mitogenome features was high, with the highest divergence occurring in protein-coding genes (average = 8.2%), followed by control region (6.7%). RNA features had lower pairwise divergences (average tRNA = 4.3%, average rRNA = 2.3%). The protein-coding ATPase 6 gene had a different stop codon between these two specimens. The high level of sequence variation between these subspecies suggests that Mesoamerican H. leucosticta might be comprised of multiple species. We urge a full phylogeographic survey of this widespread Neotropical forest bird.

Exploring the effects of salinization on trophic diversity in freshwater ecosystems: a quantitative review

Salinization of freshwater ecosystems represents a potential threat to biodiversity, but the distribution of salinity tolerance among freshwater organisms and its functional consequences are understudied. In this study, we reviewed global patterns of salinity tolerance across a broad range of freshwater organisms. Specifically, we compared published data on LC50 (a metric of salinity tolerance) across climatic regions, taxa, and functional feeding groups (FFGs). We found that microinvertebrates were more sensitive to salinity than vertebrates and macroinvertebrates. Within aquatic insects, there was considerable variability in tolerance across FFGs. Specifically, scrapers, gatherers, and filterers were more sensitive on average than omnivores, shredders, and predators. Thus, we predict that increasing salinization can negatively impact trophic diversity and in turn cause overall changes in the structure and function of freshwater ecosystems. We also identified both historical exposure and taxonomic affinity as potential drivers of contemporary salinity tolerance across freshwater organisms. Finally, we found important gaps in our understanding of the potential impacts of salinization on freshwater biodiversity, particularly in regions expected to be affected by increased salinization due to climate change and secondary salinization. Understanding the differential vulnerability of freshwater taxa is critical to predicting the ecosystem impacts of salinization, and informing conservation and management decisions.

Mitochondrial genome organization of the Ochre-bellied Flycatcher, Mionectes oleagineus

Abstract We sequenced and compared the mitogenome organization of two specimens of suboscine tyrant flycatcher Mionectes oleagineus from western and eastern Panama, representing distinct mtDNA clades. These samples show identical gene arrangement and vary in size by less than 5 base pairs. Both depict a non-standard avian gene order with an extra non-coding region (e.g. the remnant CR2), which differs in one base pair between them. Small size differences are also found on the control region and the 16S rRNA. Average uncorrected pairwise divergence among protein-coding genes (PCGs) was 2.8, ranging from 1.9% for COXIII and ND6 to 3.2% for ND2 and ATP6, respectively. These mitogenomes may be useful for understanding the evolutionary dynamics of gene order in bird mitochondrial genomes.

Low Predictability of Colour Polymorphism in Introduced Guppy (Poecilia reticulata) Populations in Panama

Colour polymorphism is a recurrent feature of natural populations, and its maintenance has been studied in a range of taxa in their native ranges. However, less is known about whether (and how) colour polymorphism is maintained when populations are removed from their native environments, as in the case of introduced species. We here address this issue by analyzing variation in colour patterns in recently-discovered introduced populations of the guppy (Poecilia reticulata) in Panama. Specifically, we use classic colour analysis to estimate variation in the number and the relative area of different colour spots across low predation sites in the introduced Panamanian range of the species. We then compare this variation to that found in the native range of the species under low- and high predation regimes. We found aspects of the colour pattern that were both consistent and inconsistent with the classical paradigm of colour evolution in guppies. On one hand, the same colours that dominated in native populations (orange, iridescent and black) were also the most dominant in the introduced populations in Panama. On the other, there were no clear differences between either introduced-low and native low- and high predation populations. Our results are therefore only partially consistent with the traditional role of female preference in the absence of predators, and suggest that additional factors could influence colour patterns when populations are removed from their native environments. Future research on the interaction between female preference and environmental variability (e.g. multifarious selection), could help understand adaptive variation in this widely-introduced species, and the contexts under which variation in adaptive traits parallels (or not) variation in the native range.