William Owen McMillan
Smithsonian Tropical Research Institute
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Featured researches published by William Owen McMillan.
Heredity | 2005
A. Tobler; Durrell D. Kapan; Nicola S. Flanagan; C Gonzalez; E. Peterson; Chris D. Jiggins; J S Johntson; David G. Heckel; William Owen McMillan
We report the first genetic linkage map of Heliconius erato, a species that shows remarkable variation in its warningly colored wing patterns. We use crosses between H. erato and its sister species, H. himera, to place two major color pattern genes, D and Cr, on a linkage map containing AFLP, allozyme, microsatellite and single-copy nuclear loci. We identified all 21 linkage groups in an initial genetic screen of 22 progeny from an F1 female × male H. himera family. Of the 229 markers, 87 used to identify linkage groups were also informative in 35 progeny from a sibling backcross (H. himera female × F1 male). With these, and an additional 33 markers informative in the second family, we constructed recombinational maps for 19 of the 21 linkage groups. These maps varied in length from 18.1 to 431.1 centimorgans (cM) and yielded an estimated total length of 2400 cM. The average distance between markers was 23 cM, and eight of the 19 linkage groups, including the sex chromosome (Z) and the chromosome containing the Cr locus, contained two or more codominant anchor loci. Of the three potential candidate genes mapped here, Cubitus interruptus (Ci), Decapentaplegic (Dpp) and Wingless (Wg), only Ci was linked, although loosely, to a known Heliconius color pattern locus. This work is an important first step for constructing a denser genetic map of the H. erato color pattern radiation and for a comparative genomic study of the architecture of mimicry in Heliconius butterflies.
Molecular Ecology | 2012
Oscar Puebla; Eldredge Bermingham; William Owen McMillan
Marine biologists have gone through a paradigm shift, from the assumption that marine populations are largely ‘open’ owing to extensive larval dispersal to the realization that marine dispersal is ‘more restricted than previously thought’. Yet, population genetic studies often reveal low levels of genetic structure across large geographic areas. On the other side, more direct approaches such as mark‐recapture provide evidence of localized dispersal. To what extent can direct and indirect studies of marine dispersal be reconciled? One approach consists in applying genetic methods that have been validated with direct estimates of dispersal. Here, we use such an approach—genetic isolation by distance between individuals in continuous populations—to estimate the spatial scale of dispersal in five species of coral reef fish presenting low levels of genetic structure across the Caribbean. Individuals were sampled continuously along a 220‐km transect following the Mesoamerican Barrier Reef, population densities were estimated from surveys covering 17 200 m2 of reef, and samples were genotyped at a total of 58 microsatellite loci. A small but positive isolation‐by‐distance slope was observed in the five species, providing mean parent‐offspring dispersal estimates ranging between 7 and 42 km (CI 1–113 km) and suggesting that there might be a correlation between minimum/maximum pelagic larval duration and dispersal in coral reef fishes. Coalescent‐based simulations indicate that these results are robust to a variety of dispersal distributions and sampling designs. We conclude that low levels of genetic structure across large geographic areas are not necessarily indicative of extensive dispersal at ecological timescales.
American Journal of Botany | 2010
Ivania Cerón-Souza; Elsie Rivera-Ocasio; Ernesto Medina; Jorge Jiménez; William Owen McMillan; Eldredge Bermingham
UNLABELLED PREMISE OF THE STUDY Hybridization is common in both animals and plants and can lead to a diverse array of outcomes ranging from the generation of new ecotypes or species to the breakdown of morphological differences. Here, we explore the extent of hybridization in the three currently recognized New World Rhizophora species-R. mangle, R. racemosa, and the putative hybrid species R. harrisonii. • METHODS We assayed variation across the three recognized Rhizophora species using two noncoding chloroplast (cpDNA), two flanking microsatellite regions (FMRs), and six microsatellite loci. • KEY RESULTS Gene genealogies of cpDNA and FMRs showed a strong phylogeographic break across the Central American Isthmus, but little relationship to recognized species boundaries. Instead, individuals collected in the same ocean basin and classified as R. mangle and R. racemosa by morphological characteristics were more closely related to each other than with similar looking individuals collected in the other ocean basin. Nonetheless, there were low, yet significant differences at microsatellite loci among co-occurring populations of R. mangle and R. racemosa in both ocean basins, suggesting that two taxonomic groups coexist. However, we found no genetic evidence that R. harrisonii was a hybrid species. Rather, R. harrisonii appears to represent a morphotype produced by ongoing hybridization and backcrossing between R. mangle and R. racemosa. • CONCLUSIONS Our data support ancient and persistent introgressive hybridization among new world Rhizophora and argue for a full revision of the systematic relationships of the group based on much finer morphological, ecological, and genetic analyses.
Molecular Ecology | 2014
Oscar Puebla; Eldredge Bermingham; William Owen McMillan
Because the vast majority of species are well diverged, relatively little is known about the genomic architecture of speciation during the early stages of divergence. Species within recent evolutionary radiations are often minimally diverged from a genomic perspective, and therefore provide rare opportunities to address this question. Here, we leverage the hamlet radiation (Hypoplectrus spp., brightly coloured reef fishes from the tropical western Atlantic) to characterize genomic divergence during the early stages of speciation. Transect surveys and spawning observations in Belize, Honduras and Panama confirm that sympatric barred (H. puella), black (H. nigricans) and butter (H. unicolor) hamlets are phenotypically distinct and reproductively isolated, although hybrid spawnings and individuals with intermediate phenotypes are seen on rare occasions. A survey of approximately 100 000 restriction site‐associated SNPs in 126 samples from the three species across the three replicate populations reveals extremely slight genomewide divergence among species (FST = 0.0038), indicating that ecomorphological differences and functional reproductive isolation are maintained in sympatry in a backdrop of extraordinary genomic similarity. Nonetheless, a very small proportion of SNPs (0.05% on average) are identified as FST outliers among sympatric species. Remarkably, a single SNP is identified as an outlier in repeated populations for the same species pair. A minicontig assembled de novo around this SNP falls into the genomic region containing the HoxCa10 and HoxCa11 genes in 10 teleost species, suggesting an important role for Hox gene evolution in this radiation. This finding, if confirmed, would provide a better understanding of the links between micro‐ and macroevolutionary processes.
BMC Evolutionary Biology | 2012
Ivania Cerón-Souza; Eldredge Bermingham; William Owen McMillan; Frank A. Jones
BackgroundMangroves 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.ResultsBoth 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 (Hd= 0.8 > 0.2) than R. mangle. The Central American Isthmus serves as an exceptionally strong barrier to gene flow, with high levels nuclear (FST= 0.3-0.5) and plastid (FST= 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.ConclusionsWe 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.
Molecular Ecology | 2012
Carlos F. Arias; Claudia Rosales; Camilo Salazar; Jully Castaño; Eldredge Bermingham; Mauricio Linares; William Owen McMillan
Hybrid zones are powerful natural systems to study evolutionary processes to gain an understanding of adaptation and speciation. In the Cauca Valley (Colombia), two butterfly races, Heliconius cydno cydnides and Heliconius cydno weymeri, meet and hybridize. We characterized this hybrid zone using a combination of mitochondrial DNA (mtDNA) sequences, amplified fragment length polymorphisms (AFLPs), microsatellites and sequences for nuclear loci within and outside of the genomic regions that cause differences in wing colour pattern. The hybrid zone is largely composed of individuals of mixed ancestry. However, there is strong genetic discontinuity between the hybridizing races in mtDNA and, to a lesser extent, in all nuclear markers surveyed. The mtDNA clustering of H. c. cydnides with the H. cydno race from the Magdalena Valley and H. c. weymeri with the H. cydno race from the pacific coast suggests that H. c. cydnides colonized the Cauca Valley from the north, whereas H. c. weymeri did so by crossing the Andes in the southern part, implying a secondary contact origin. Colonization of the valley by H. cydno was accompanied by mimicry shift. Strong ecological isolation, driven by locally adaptive differences in mimetic wing patterns, is playing an important role in maintaining the hybrid zone. However, selection on wing pattern alone is not sufficient to explain the genetic discontinuity observed. There is evidence for differences in male mating preference, but the contribution of additional barriers needs further investigation. Overall, our results support the idea that speciation is a cumulative process, where the combination of multiple isolation barriers, combined with major phenotypic differences, facilitates population divergence in face of gene flow.
BMC Evolutionary Biology | 2015
Megan A. Supple; Riccardo Papa; Heather M. Hines; William Owen McMillan; Brian A. Counterman
BackgroundA key to understanding the origins of species is determining the evolutionary processes that drive the patterns of genomic divergence during speciation. New genomic technologies enable the study of high-resolution genomic patterns of divergence across natural speciation continua, where taxa pairs with different levels of reproductive isolation can be used as proxies for different stages of speciation. Empirical studies of these speciation continua can provide valuable insights into how genomes diverge during speciation.MethodsWe examine variation across a handful of genomic regions in parapatric and allopatric populations of Heliconius butterflies with varying levels of reproductive isolation. Genome sequences were mapped to 2.2-Mb of the H. erato genome, including 1-Mb across the red color pattern locus and multiple regions unlinked to color pattern variation.ResultsPhylogenetic analyses reveal a speciation continuum of pairs of hybridizing races and incipient species in the Heliconius erato clade. Comparisons of hybridizing pairs of divergently colored races and incipient species reveal that genomic divergence increases with ecological and reproductive isolation, not only across the locus responsible for adaptive variation in red wing coloration, but also at genomic regions unlinked to color pattern.DiscussionWe observe high levels of divergence between the incipient species H. erato and H. himera, suggesting that divergence may accumulate early in the speciation process. Comparisons of genomic divergence between the incipient species and allopatric races suggest that limited gene flow cannot account for the observed high levels of divergence between the incipient species.ConclusionsOur results provide a reconstruction of the speciation continuum across the H. erato clade and provide insights into the processes that drive genomic divergence during speciation, establishing the H. erato clade as a powerful framework for the study of speciation.
bioRxiv | 2015
Nicola J. Nadeau; Carolina Pardo-Diaz; Annabel Whibley; Megan A. Supple; Richard W. R. Wallbank; Grace C. Wu; Luana S. Maroja; Laura Ferguson; Heather M. Hines; Camilo Salazar; Richard H. ffrench-Constant; Mathieu Joron; William Owen McMillan; Chris D. Jiggins
A major challenge in evolutionary biology is to understand the origins of novel structures. The wing patterns of butterflies and moths are derived phenotypes unique to the Lepidoptera. Here we identify a gene that we name poikilomousa (poik), which regulates colour pattern switches in the mimetic Heliconius butterflies. Strong associations between phenotypic variation and DNA sequence variation are seen in three different Heliconius species, in addition to associations between gene expression and colour pattern. Colour pattern variants are also associated with differences in splicing of poik transcripts. poik is a member of the conserved fizzy family of cell cycle regulators. It belongs to a faster evolving subfamily, the closest functionally characterised orthologue being the cortex gene in Drosophila, a female germ-line specific protein involved in meiosis. poik appears to have adopted a novel function in the Lepidoptera and become a major target for natural selection acting on colour and pattern variation in this group.
Proceedings of the Royal Society B-Biological Sciences, 283 (1844). p. 20161821. | 2016
L. Theodosiou; William Owen McMillan; Oscar Puebla
When there is no recombination (achiasmy) in one sex, it is in the heterogametic one. This observation is so consistent that it constitutes one of the few patterns in biology that may be regarded as a ‘rule’ and Haldane (Haldane 1922 J. Genet. 12, 101–109. (doi:10.1007/BF02983075)) proposed that it might be driven by selection against recombination in the sex chromosomes. Yet differences in recombination rates between the sexes (heterochiasmy) have also been reported in hermaphroditic species that lack sex chromosomes. In plants—the vast majority of which are hermaphroditic—selection at the haploid stage has been proposed to drive heterochiasmy. Yet few data are available for hermaphroditic animals, and barely any for hermaphroditic vertebrates. Here, we leverage reciprocal crosses between two black hamlets (Hypoplectrus nigricans, Serranidae), simultaneously hermaphroditic reef fishes from the wider Caribbean, to generate high-density egg- and sperm-specific linkage maps for each parent. We find globally higher recombination rates in the eggs, with dramatically pronounced heterochiasmy at the chromosome peripheries. We suggest that this pattern may be due to female meiotic drive, and that this process may be an important source of heterochiasmy in animals. We also identify a large non-recombining region that may play a role in speciation and local adaptation in Hypoplectrus.
Ecology and Evolution | 2018
Timothy J. Thurman; Emily Brodie; Elizabeth Evans; William Owen McMillan
Abstract 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.