Dr. Robin Hopkins

Dr. Robin Hopkins

A major goal of our research is to link genotype to phenotype in the process of adaptation and the evolution of reproductive isolation. We study how traits that contribute to reproductive isolation and adaptation evolve through the interaction of migration, drift, and selection. Our work focuses on Phlox, a charismatic genus of flowering plants with a rich history of ecological and evolutionary study. We use Phlox to investigate an ever-increasing range of topics including plant-pollinator interactions, the evolution of self-incompatibility, and the process of reinforcement.

Reinforcement


Reinforcement

Reinforcement is the process by which reduced hybrid fitness generates selection for the evolution of reproductive isolation between emerging species. This is an important way in which natural selection can contribute to the process of speciation. We use molecular biology, population genetic analyses, and field-based selection experiments to investigate reinforcement in two Texas wildflowers, Phlox drummondii and Phlox cuspidata.

The distribution of Phlox drummondii and Phlox cuspidata throughout Texas. Both species have light blue flowers throughout most of their ranges, but P. drummondii has dark red flowers in the region where both species co-occur.

The distribution of Phlox drummondii and Phlox cuspidata throughout Texas. Both species have light blue flowers throughout most of their ranges, but P. drummondii has dark red flowers in the region where both species co-occur.

Both species of Phlox produce light blue flowers throughout most of their ranges, but P. drummondii has dark red flowers in eastern populations that are sympatric with P. cuspidata. Our work has shown that this change in flower color is caused by reinforcement. Using common garden field experiments, we determined that dark-red flowered plants produce nearly half as many hybrids as light-blue flowered plants. Hybrids have high sterility and therefore this reduction in hybridization is favored by reinforcing selection. This work represents the first time reinforcement was measured under natural field conditions.

We followed up this work by estimating the strength of reinforcing selection acting on flower color variation. We combined field observations of the change in flower color over geographic space with a spatially explicit population genetic model. Our results indicate that selection is very strong and acts to favor dark red flowers in sympatric populations and light blue flowers in allopatric populations.

Related Publications

Gene flow during reinforcement

Roda, Federico, Fábio K. Mendes, Matthew W. Hahn, and Robin Hopkins. 2017. Genomic evidence of gene flow during reinforcement in Texas Phlox. Molecular Ecology 26: 2317-2330. [PDF]

Strong reinforcing selection in a Texas wildflower.

Hopkins, Robin, Rafael F. Guerrero, Mark D. Rausher, Mark Kirkpatrick. Strong reinforcing selection in a Texas wildflower. 2014. Current Biology 24:1995-1999. (Featured in Current Biology Dispatch by Daniel Matute and Daniel Ortiz-Barrientos) [PDF]

The cost of reinforcement: Selection on flower color in allopatric populations of Phlox drummondii.

Hopkins, Robin, Rausher, Mark D. The cost of reinforcement: Selection on flower color in allopatric populations of Phlox drummondii. 2014. The American Naturalist 183: 693-710. [PDF]

2013 Reinforcement in plants.

Hopkins, Robin. 2013 Reinforcement in plants. New Phytologist 197: 1095-1103 [PDF]

Pollinator-mediated selection on flower color allele drives reinforcement

Hopkins, Robin, Mark D. Rausher. 2012. Pollinator-mediated selection on flower color allele drives reinforcement. Science 335: 1090-1092. (Featured in Current Biology Dispatch by John Pannell) [PDF]

Molecular signatures of selection on reproductive character displacement of flower color in Phlox drummondii

Hopkins, Robin, Donald A. Levin, Mark D. Rausher. 2012. Molecular signatures of selection on reproductive character displacement of flower color in Phlox drummondii. Evolution 66:469-485 [PDF]

Genetics & Genomics of Speciation

Genetics & Genomics of Speciation

Flower color variation in Phlox drummondii is controlled by two loci. The hue locus (h/H) controls the type of pigments produced in the flower with a red allele that is recessive to a blue allele. The intensity locus (i/I) controls the amount of pigment produced in the flower with a light allele recessive to a dark allele. Four possible flower colors result from variation at these two loci.

Flower color variation in Phlox drummondii is controlled by two loci. The hue locus (h/H) controls the type of pigments produced in the flower with a red allele that is recessive to a blue allele. The intensity locus (i/I) controls the amount of pigment produced in the flower with a light allele recessive to a dark allele. Four possible flower colors result from variation at these two loci.

Identifying the genetic changes causing reproductive isolation can greatly enhance our understanding of the process of speciation. We can use knowledge about the genetic changes causing speciation to investigate the role of evolutionary processes such as selection, migration, epistasis, and pleiotropy in speciation.

We have identified the genes causing reinforcement in Phlox. Flower color variation in P. drummondii is caused by two loci: one corresponds to the enzyme Flavonoid 3’5’-hydroxylase which changes flower hue from blue to red, and the other corresponds to an R2R3-Myb transcription factor which changes flower color intensity from light to dark. Gene expression analyses demonstrated that cis-regulatory mutations underlie the variation at both loci and result in expression change of key enzymes in the anthocyanin biosynthesis pathway. Interestingly, the simple genetic basis of reinforcement in Phlox, involving cis-regulatory mutations in just a few loci, is similar to other cases of flower color evolution in which reinforcement is not known to be involved. Our future work aims to identify the actual mutations causing the cis-regulatory changes in these two flower color genes.

Once we identify the mutations causing reinforcement in Phlox we will use sequence variation surrounding the causal mutations to understand the role of selection during the evolution of reproductive isolation. We aim to distinguish between models of selection from standing genetic variation and single de novo mutation.

The Phlox system provides a unique opportunity to investigate hybridization during reinforcement. It is becoming increasingly clear that hybridization and introgression play an important and dynamic role in the process of species formation. An emerging area of genomic analysis focuses on identifying and understanding genomic introgression. These analyses have been used to differentiate between introgression and incomplete lineage sorting, to estimate relative rates of introgression, and to determine the direction of introgression. We aim to use these analyses to better understand the role of hybridization and introgression during the process of reinforcement in Phlox.

Related Publications

Molecular signatures of selection on reproductive character displacement of flower color in Phlox drummondii

Hopkins, Robin, Donald A. Levin, Mark D. Rausher. 2012. Molecular signatures of selection on reproductive character displacement of flower color in Phlox drummondii. Evolution 66:469-485 [PDF]

Identification of two genes causing reinforcement in the Texas wildflower Phlox drummondii

Hopkins, Robin, Mark D. Rausher. 2011. Identification of two genes causing reinforcement in the Texas wildflower Phlox drummondii. Nature 469:411-414. [PDF]

Self-incompatibility & Inter-specific Incompatibility

Self-incompatibility & Interspecific Incompatibility

Most flowering plants have mechanisms to impede fertilization by self-pollination and by pollen from different species. These self-incompatibility and interspecific-incompatibility systems maintain plant diversity by promoting out-crossing and impeding hybridization. It has been suggested that self-incompatibility and interspecific-incompatibility involve common pathways but evidence for this link is incomplete.

Pollen germination

Pollen germination

We aim to exploit variation for self-incompatibility and interspecific-incompatibility in Phlox to determine if there is a link between these two reproductive barriers. Phlox cuspidata is a self-compatible species where as Phlox drummondii is largely self-incompatible, although there is documented variation in the amount of self-incompatibility. The two species also show variation in the amount of interspecific compatibility.

We are interested in determining if there is a correlation between levels of self-incompatibility and levels of interspecific-incompatibility in Phlox. By examining pollen germination and growth during self-crosses and interspecific crosses we aim to determine if self-incompatibility and interspecific-incompatibility follow similar developmental trajectories. Finally, we will use genetic mapping to determine if the two incompatibility systems have overlapping genetic bases.

Pollinator Behavior

Pollinator Behavior

Pipevine swallowtail (Battus philenor) pollinating a Phlox drummondii flower

Pipevine swallowtail (Battus philenor) pollinating a Phlox drummondii flower

Understanding selection at a detailed mechanistic level involves in-depth investigations of how organisms interact with each other and their environment. It is becoming increasingly clear that the adaptive value of a trait can be dependent on interactions between organisms. Our research explores plant-pollinator interactions to better understand the eco-evolutionary dynamics of multi-species interactions.

The lab focuses on investigating pollinator behavioral response to flower color variation in Phlox. Both P. drummondii and P. cuspidata are pollinated by the same array of butterfly species. The predominant pollinator of Phlox, the pipevine swallowtail (Battus philenor), shows both constancy and preference based on flower color. Our work indicates that B. philenor prefer light and blue flowered Phlox to dark and red flowered Phlox. This preference is likely responsible for maintaining the ancestral flower color in allopatric populations. Individual pollinators also show constancy based on flower color when foraging between species. In other words, a butterfly will move between the two Phlox species when they have the same flower color but less so when they have different flower colors. This foraging constancy causes reproductive isolation between the two Phlox when they have different flower colors.

We are interested in expanding this pollinator work to explore how pollinator behavior (both preference and constancy) varies due to learning over time. Previous work on Battus indicates they are capable of learning color and this learning can influence the strength and direction of preference. We aim to identify what aspects of color are learned and how this learning influences the strength of preference on Phlox flower color.

Pollinator observation results from arrays of Phlox drummondii and Phlox cuspidata plants. Arrows indicate observed movements of butterflies between species of plants. Orange arrows indicate movement from P. drummondii to P. cuspidata and green arrows indicate movement from P. cuspidata to P. drummondii. The percent of the total movement observed for each pair of flowers is shown in the corresponding arrow.

Pollinator observation results from arrays of Phlox drummondii and Phlox cuspidata plants. Arrows indicate observed movements of butterflies between species of plants. Orange arrows indicate movement from P. drummondii to P. cuspidata and green arrows indicate movement from P. cuspidata to P. drummondii. The percent of the total movement observed for each pair of flowers is shown in the corresponding arrow.

Our research will also explore how pollinator preference and constancy vary due to frequency of floral signal. Previous studies have reported frequency dependent selection on floral traits. We are interested in exploring if frequency dependent pollinator behavior underlies this selection. We aim to quantify pollinator preference and constancy in arrays of Phlox with different frequencies to understand how the strength of selection varies across populations with different frequencies of flower color morphs.

Related Publications

The cost of reinforcement: Selection on flower color in allopatric populations of Phlox drummondii.

Hopkins, Robin, Rausher, Mark D. The cost of reinforcement: Selection on flower color in allopatric populations of Phlox drummondii. 2014. The American Naturalist 183: 693-710. [PDF]

Pollinator-mediated selection on flower color allele drives reinforcement

Hopkins, Robin, Mark D. Rausher. 2012. Pollinator-mediated selection on flower color allele drives reinforcement. Science 335: 1090-1092. (Featured in Current Biology Dispatch by John Pannell) [PDF]