Comparative phylogeography can elucidate the influence of historical events on current patterns of biodiversity and can identify patterns of co-vicariance among unrelated taxa that span the same geographic areas. Here we analyze temporal and spatial divergence patterns of cloud forest plant and animal species and relate them to the evolutionary history of naturally fragmented cloud forests–among the most threatened vegetation types in northern Mesoamerica. We used comparative phylogeographic analyses to identify patterns of co-vicariance in taxa that share geographic ranges across cloud forest habitats and to elucidate the influence of historical events on current patterns of biodiversity. We document temporal and spatial genetic divergence of 15 species (including seed plants, birds and rodents), and relate them to the evolutionary history of the naturally fragmented cloud forests. We used fossil-calibrated genealogies, coalescent-based divergence time inference, and estimates of gene flow to assess the permeability of putative barriers to gene flow. We also used the hierarchical Approximate Bayesian Computation (HABC) method implemented in the program msBayes to test simultaneous versus non-simultaneous divergence of the cloud forest lineages. Our results show shared phylogeographic breaks that correspond to the Isthmus of Tehuantepec, Los Tuxtlas, and the Chiapas Central Depression, with the Isthmus representing the most frequently shared break among taxa. However, dating analyses suggest that the phylogeographic breaks corresponding to the Isthmus occurred at different times in different taxa. Current divergence patterns are therefore consistent with the hypothesis of broad vicariance across the Isthmus of Tehuantepec derived from different mechanisms operating at different times. This study, coupled with existing data on divergence cloud forest species, indicates that the evolutionary history of contemporary cloud forest lineages is complex and often lineage-specific, and thus difficult to capture in a simple conservation strategy.
The adaptiveness of distyly has been typically investigated in terms of its female function, specifically pollen receipt. However, pollen loads on stigmas can only provide moderate support for Darwin's hypothesis of the promotion of legitimate crosses. To determine the effectiveness of hummingbirds as pollen vectors between floral morphs and the consequences in terms of male (pollen transfer) and female function (pollen receipt) in Palicourea padifolia (Rubiaceae), floral visitors, their foraging modes, and temporal patterns of floral visitation were observed and documented. Differences in pollen and stigma morphology, pollen flow, rates of pollen deposition, and/or stigmatic pollen loads were then evaluated for their contribution toward differences in reproductive output between floral morphs. A pollination experiment with stuffed hummingbirds that varied in bill size was done to evaluate the contribution of bill variation toward differences between floral morphs in pollen receipt and pollen transfer and female reproductive output. Anthers of long-styled flowers contained significantly more and smaller pollen grains than those of short-styled flowers, independently of corolla and anther lengths. The shape and orientation of the stigma lobes differed between morphs and were significantly longer among short-styled flowers. Hummingbird visitation rates did not differ significantly between floral morphs, and foraging movements from focal plants towards neighboring plants were independent of floral morph. Stigmatic pollen loads under field conditions and those after controlled hummingbird visitation, along with rates of pollen accumulation through the day indicated that stigmas of short-styled flowers receive proportionately more legitimate (intermorph) pollen grains than did those of long-styled flowers. However, the species of hummingbird was marginally significant in explaining variation in pollen deposition on stigmas. Lastly, intermorph pollinations of P. padifolia resulted in significant differences in fruit production between floral morphs, independent of pollination treatment and pollinator species; short-styled flowers proportionately developed almost twice the number of fruits developed by long-styled flowers.
By definition, the floral morphs of distylous plants differ in floral architecture. Yet, because cross-pollination is necessary for reproductive success in both morphs, they should not differ in attributes that contribute to attracting and rewarding floral visitors. Floral and vegetative attributes that function in distylous polymorphism in hummingbird-pollinated Palicourea padifolia (Rubiaceae) and the responses of pollinators and insect herbivores to the resources offered by both morphs were investigated. The performance of each morph along multiple stages of the reproductive cycle, from inflorescence and nectar production to fruit production, was surveyed, and pollinator behavior and nectar standing crops were then observed. Costs associated with such attractiveness were also evaluated in terms of herbivore attack and of plant reproductive fitness (female function) as a function of leaf herbivory. The number of inflorescences, floral buds, open flowers, and ripe fruits offered by either floral morph were similar, but short-styled plants almost doubled the number of developing fruits of long-styled plants. Long-styled flowers produced higher nectar volumes and accumulated more nectar over time than short-styled flowers. Measures of nectar standing crop and data on pollinator behavior suggest that hummingbirds respond to this morph-specific scheduling of nectar production. Lastly, long-styled plants suffered a higher herbivore attack and lost more leaf area over time than those with short-styled flowers. Herbivory was negatively correlated with fruit number and fruit mass, and long-styled plants set significantly less fruit mass than short-styled plants. The results suggest that pollinators and herbivores may exert selective pressures on floral and vegetative traits that could also influence gender function.
BackgroundMesoamerica is one of the most threatened biodiversity hotspots in the world, yet we are far from understanding the geologic history and the processes driving population divergence and speciation for most endemic taxa. In species with highly differentiated populations selective and/or neutral factors can induce rapid changes to traits involved in mate choice, promoting reproductive isolation between allopatric populations that can eventually lead to speciation. We present the results of genetic differentiation, and explore drift and selection effects in promoting acoustic and morphological divergence among populations of Campylopterus curvipennis, a lekking hummingbird with an extraordinary vocal variability across Mesoamerica.ResultsAnalyses of two mitochondrial genes and ten microsatellite loci genotyped for 160 individuals revealed the presence of three lineages with no contemporary gene flow: C. c. curvipennis, C. c. excellens, and C. c. pampa disjunctly distributed in the Sierra Madre Oriental, the Tuxtlas region and the Yucatan Peninsula, respectively. Sequence mtDNA and microsatellite data were congruent with two diversification events: an old vicariance event at the Isthmus of Tehuantepec (c. 1.4 Ma), and a more recent Pleistocene split, isolating populations in the Tuxtlas region. Hummingbirds of the excellens group were larger, and those of the pampa group had shorter bills, and lineages that have been isolated the longest shared fewer syllables and differed in spectral and temporal traits of a shared syllable. Coalescent simulations showed that fixation of song types has occurred faster than expected under neutrality but the null hypothesis that morphological divergence resulted from drift was not rejected.ConclusionsOur phylogeographic analyses uncovered the presence of three Mesoamerican wedge-tailed sabrewing lineages, which diverged at different time scales. These results highlight the importance of the Isthmus of Tehuantepec and more recent Pleistocene climatic events in driving isolation and population divergence. Coalescent analyses of the evolution of phenotypic traits suggest that selection is driving song evolution in wedge-tailed sabrewings but drift could not be rejected as a possibility for morphological divergence.
BackgroundEcological adaptation to host taxa is thought to result in mistletoe speciation via race formation. However, historical and ecological factors could also contribute to explain genetic structuring particularly when mistletoe host races are distributed allopatrically. Using sequence data from nuclear (ITS) and chloroplast (trnL-F) DNA, we investigate the genetic differentiation of 31 Psittacanthus schiedeanus (Loranthaceae) populations across the Mesoamerican species range. We conducted phylogenetic, population and spatial genetic analyses on 274 individuals of P. schiedeanus to gain insight of the evolutionary history of these populations. Species distribution modeling, isolation with migration and Bayesian inference methods were used to infer the evolutionary transition of mistletoe invasion, in which evolutionary scenarios were compared through posterior probabilities.ResultsOur analyses revealed shallow levels of population structure with three genetic groups present across the sample area. Nine haplotypes were identified after sequencing the trnL-F intergenic spacer. These haplotypes showed phylogeographic structure, with three groups with restricted gene flow corresponding to the distribution of individuals/populations separated by habitat (cloud forest localities from San Luis Potosí to northwestern Oaxaca and Chiapas, localities with xeric vegetation in central Oaxaca, and localities with tropical deciduous forests in Chiapas), with post-glacial population expansions and potentially corresponding to post-glacial invasion types. Similarly, 44 ITS ribotypes suggest phylogeographic structure, despite the fact that most frequent ribotypes are widespread indicating effective nuclear gene flow via pollen. Gene flow estimates, a significant genetic signal of demographic expansion, and range shifts under past climatic conditions predicted by species distribution modeling suggest post-glacial invasion of P. schiedeanus mistletoes to cloud forests. However, Approximate Bayesian Computation (ABC) analyses strongly supported a scenario of simultaneous divergence among the three groups isolated recently.ConclusionsOur results provide support for the predominant role of isolation and environmental factors in driving genetic differentiation of Mesoamerican parrot-flower mistletoes. The ABC results are consistent with a scenario of post-glacial mistletoe invasion, independent of host identity, and that habitat types recently isolated P. schiedeanus populations, accumulating slight phenotypic differences among genetic groups due to recent migration across habitats. Under this scenario, climatic fluctuations throughout the Pleistocene would have altered the distribution of suitable habitat for mistletoes throughout Mesoamerica leading to variation in population continuity and isolation. Our findings add to an understanding of the role of recent isolation and colonization in shaping cloud forest communities in the region.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0648...
Aim We used mitochondrial DNA sequences to reconstruct the phylogenetic relationships of Mesoamerican Amazilia hummingbirds (Trochilidae). The phylogeny was used to identify vicariance scenarios, reconstruct ancestral biogeographical areas, and investigate the role of geological events in generating genetic divergence through vicariance events.Location Mesoamerica.Methods Molecular sequence data were gathered from three mitochondrial genes (ND2, ND5 and 12S) for samples taken within the Mesoamerican region and analysed using maximum parsimony, maximum-likelihood and Bayesian approaches. Statistical dispersal-vicariance analysis (S-DIVA) was used to reconstruct biogeographical areas and changes in distribution during the evolutionary history of Amazilia. The phylogeny was calibrated using fossil dates, mean substitution rates and coalescent-based divergence time inference.Results Amazilia can be split into two divergent lineages, with high levels of sequence divergence within some Mesoamerican species. Ancestral area reconstructions favour an ancestral distribution west of the Isthmus of Tehuantepec, with subsequent dispersals east of the isthmus and to South America. Divergence time estimations suggest that major diversification events occurred in the Miocene and Pliocene, corresponding temporally and geographically to the formation of the mountain systems and establishment of the major biomes in Mesoamerica. Main conclusionsThe diversification of Amazilia corresponds to vegetation shifts in combination with regional orogenesis. Intriguingly, the timing of the major diversification events and dispersal into South America pre-dates the completion of the Panamanian isthmus c. 4 Ma before present.
The costs of bird song incurred in a diversity of ways may result in trade‐offs in the production and maintenance of elaborate plumage ornaments. In this paper, we examine evolutionary trade‐offs between acoustic and visual signalling in trogon birds (Trogonidae). Using multiple regressions with phylogenetically independent contrasts, we found that interspecific variation in male plumage coloration was not significantly predicted by song traits (reduced by PCA) or altitude. Although plumage coloration is expected to decrease with increases in song elaboration, both groups of variables were not related. Given that song and plumage coloration traits are likely targets of sexual selection, we also examined their relationships with sexual plumage dimorphism. We found that male carotenoid‐derived coloration was positively related to sexual plumage dimorphism, suggesting that sexual selection on male carotenoid‐derived coloration may be stronger than on melanin‐ or structurally based coloration, or than on acoustic traits. Comparative studies on other bird families accounting for the effects of phylogeny as well as environmental covariates are required to test the generality of our findings in trogons.
The prevalent view on genetic structuring in parasitic plants is that host-race formation is caused by varying degrees of host specificity. However, the relative importance of ecological niche divergence and host specificity to population differentiation remains poorly understood. We evaluated the factors associated with population differentiation in mistletoes of the Psittacanthus schiedeanus complex (Loranthaceae) in Mexico. We used genetic data from chloroplast sequences and nuclear microsatellites to study population genetic structure and tested its association with host preferences and climatic niche variables. Pairwise genetic differentiation was associated with environmental and host preferences, independent of geography. However, environmental predictors appeared to be more important than host preferences to explain genetic structure, supporting the hypothesis that the occurrence of the parasite is largely determined by its own climatic niche and, to a lesser degree, by host specificity. Genetic structure is significant within this mistletoe species complex, but the processes associated with this structure appear to be more complex than previously thought. Although host specificity was not supported as the major determinant of population differentiation, we consider this to be part of a more comprehensive ecological model of mistletoe host-race formation that incorporates the effects of climatic niche evolution.
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