Climate anomalies and competition reduce establishment success during island colonization.

Understanding the factors that facilitate or constrain establishment of populations in novel environments is crucial for conservation biology and the study of adaptive radiation. Important questions include: (1) Does the timing of colonization relative to stochastic events, such as climatic perturbations, impact the probability of successful establishment? (2) To what extent does community context (e.g., the presence of competitors) change the probability of establishment? (3) How do sources of intrapopulation variance, such as sex differences, affect success at an individual level during the process of establishment? Answers to these questions are rarely pursued in a field-experimental context or on the same time scales (months to years) as the processes of colonization and establishment. We introduced slender anole lizards (Anolis apletophallus) to eight islands in the Panama Canal and tracked them over multiple generations to investigate the factors that mediate establishment success. All islands were warmer than the mainland (ancestral) environment, and some islands had a native competitor. We transplanted half of these populations only 4 months before the onset of a severe regional drought and the other half 2 years (two generations) before the drought. We found that successful establishment depended on both the intensity of interspecific competition and the timing of colonization relative to the drought. The islands that were colonized shortly before the drought went functionally extinct by the second generation, and regardless of time before the drought, the populations on islands with interspecific competition declined continuously over the study period. Furthermore, the effect of the competitor interacted with sex, with males suffering, and females benefitting, from the presence of a native competitor. Our results reveal that community context and the timing of colonization relative to climactic events can combine to determine establishment success and that these factors can generate opposite effects on males and females.

Scale-dependent environmental effects on phenotypic distributions in Heliconius butterflies.

Identifying the relative importance of different mechanisms responsible for the emergence and maintenance of phenotypic diversity can be challenging, as multiple selective pressures and stochastic events are involved in these processes. Therefore, testing how environmental conditions shape the distribution of phenotypes can offer important insights on local adaptation, divergence, and speciation. The red-yellow Müllerian mimicry ring of Heliconius butterflies exhibits a wide diversity of color patterns across the Neotropics and is involved in multiple hybrid zones, making it a powerful system to investigate environmental drivers of phenotypic distributions. Using the distantly related Heliconius erato and Heliconius melpomene co-mimics and a multiscale distribution approach, we investigated whether distinct phenotypes of these species are associated with different environmental conditions. We show that Heliconius red-yellow phenotypic distribution is strongly driven by environmental gradients (especially thermal and precipitation variables), but that phenotype and environment associations vary with spatial scale. While co-mimics are usually predicted to occur in similar environments at large spatial scales, patterns at local scales are not always consistent (i.e., different variables are best predictors of phenotypic occurrence in different locations) or congruent (i.e., co-mimics show distinct associations with environment). We suggest that large-scale analyses are important for identifying how environmental factors shape broad mimetic phenotypic distributions, but that local studies are essential to understand the context-dependent biotic, abiotic, and historical mechanisms driving finer-scale phenotypic transitions.

The evolution of microendemism in a reef fish (Hypoplectrus maya).

Marine species tend to have extensive distributions, which are commonly attributed to the dispersal potential provided by planktonic larvae and the rarity of absolute barriers to dispersal in the ocean. Under this paradigm, the occurrence of marine microendemism without geographic isolation in species with planktonic larvae poses a dilemma. The recently described Maya hamlet (Hypoplectrus maya, Serranidae) is exactly such a case, being endemic to a 50-km segment of the Mesoamerican Barrier Reef System (MBRS). We use whole-genome analysis to infer the demographic history of the Maya hamlet and contrast it with the sympatric and pan-Caribbean black (H. nigricans), barred (H. puella) and butter (H. unicolor) hamlets, as well as the allopatric but phenotypically similar blue hamlet (H. gemma). We show that H. maya is indeed a distinct evolutionary lineage, with genomic signatures of inbreeding and a unique demographic history of continuous decrease in effective population size since it diverged from congeners just ~3,000 generations ago. We suggest that this case of microendemism may be driven by the combination of a narrow ecological niche and restrictive oceanographic conditions in the southern MBRS, which is consistent with the occurrence of an unusually high number of marine microendemics in this region. The restricted distribution of the Maya hamlet, its decline in both census and effective population sizes, and the degradation of its habitat place it at risk of extinction. We conclude that the evolution of marine microendemism can be a fast and dynamic process, with extinction possibly occurring before speciation is complete.

Facultative pupal mating in Heliconius erato: Implications for mate choice, female preference, and speciation.

Mating systems have broad impacts on how sexual selection and mate choice operate within a species, but studies of mating behavior in the laboratory may not reflect how these processes occur in the wild. Here, we examined the mating behavior of the neotropical butterfly Heliconius erato in the field by releasing larvae and virgin females and observing how they mated. H. erato is considered a pupal-mating species (i.e., males mate with females as they emerge from the pupal case). However, we observed only two teneral mating events, and experimentally released virgins were almost all mated upon recapture. Our study confirms the presence of some pupal-mating behavior in H. erato, but suggests that adult mating is likely the prevalent mating strategy in this species. These findings have important implications for the role of color pattern and female mate choice in the generation of reproductive isolation in this diverse genus.

Comparative Genomics Reveals Accelerated Evolution in Conserved Pathways during the Diversification of Anole Lizards.

Squamates include all lizards and snakes, and display some of the most diverse and extreme morphological adaptations among vertebrates. However, compared with birds and mammals, relatively few resources exist for comparative genomic analyses of squamates, hampering efforts to understand the molecular bases of phenotypic diversification in such a speciose clade. In particular, the ∼400 species of anole lizard represent an extensive squamate radiation. Here, we sequence and assemble the draft genomes of three anole species-Anolis frenatus, Anolis auratus, and Anolis apletophallus-for comparison with the available reference genome of Anolis carolinensis. Comparative analyses reveal a rapid background rate of molecular evolution consistent with a model of punctuated equilibrium, and strong purifying selection on functional genomic elements in anoles. We find evidence for accelerated evolution in genes involved in behavior, sensory perception, and reproduction, as well as in genes regulating limb bud development and hindlimb specification. Morphometric analyses of anole fore and hindlimbs corroborated these findings. We detect signatures of positive selection across several genes related to the development and regulation of the forebrain, hormones, and the iguanian lizard dewlap, suggesting molecular changes underlying behavioral adaptations known to reinforce species boundaries were a key component in the diversification of anole lizards.

Evolution of novel mimicry rings facilitated by adaptive introgression in tropical butterflies.

Understanding the genetic basis of phenotypic variation and the mechanisms involved in the evolution of adaptive novelty, especially in adaptive radiations, is a major goal in evolutionary biology. Here, we used whole-genome sequence data to investigate the origin of the yellow hindwing bar in the Heliconius cydno radiation. We found modular variation associated with hindwing phenotype in two narrow noncoding regions upstream and downstream of the cortex gene, which was recently identified as a pigmentation pattern controller in multiple species of Heliconius. Genetic variation at each of these modules suggests an independent control of the dorsal and ventral hindwing patterning, with the upstream module associated with the ventral phenotype and the downstream module with the dorsal one. Furthermore, we detected introgression between H. cydno and its closely related species Heliconius melpomene in these modules, likely allowing both species to participate in novel mimicry rings. In sum, our findings support the role of regulatory modularity coupled with adaptive introgression as an elegant mechanism by which novel phenotypic combinations can evolve and fuel an adaptive radiation.

Comparative genetic structure of two mangrove species in Caribbean and Pacific estuaries of Panama.

BACKGROUND: Mangroves are ecologically important and highly threatened forest communities. Observational and genetic evidence has confirmed the long distance dispersal capacity of water-dispersed mangrove seeds, but less is known about the relative importance of pollen vs. seed gene flow in connecting populations. We analyzed 980 Avicennia germinans for 11 microsatellite loci and 940 Rhizophora mangle for six microsatellite loci and subsampled two non-coding cpDNA regions in order to understand population structure, and gene flow within and among four major estuaries on the Caribbean and Pacific coasts of Panama. RESULTS: Both species showed similar rates of outcrossing (t= 0.7 in A. germinans and 0.8 in R. mangle) and strong patterns of spatial genetic structure within estuaries, although A. germinans had greater genetic structure in nuclear and cpDNA markers (7 demes > 4 demes and Sp= 0.02 > 0.002), and much greater cpDNA diversity (H(d)= 0.8 > 0.2) than R. mangle. The Central American Isthmus serves as an exceptionally strong barrier to gene flow, with high levels nuclear (F(ST)= 0.3-0.5) and plastid (F(ST)= 0.5-0.8) genetic differentiation observed within each species between coasts and no shared cpDNA haplotypes between species on each coast. Finally, evidence of low ratios of pollen to seed dispersal (r = -0.6 in A. germinans and 7.7 in R. mangle), coupled with the strong observed structure in nuclear and plastid DNA among most estuaries, suggests low levels of gene flow in these mangrove species. CONCLUSIONS: We conclude that gene dispersal in mangroves is usually limited within estuaries and that coastal geomorphology and rare long distance dispersal events could also influence levels of structure.