Mechanisms of reinforcement in natural and simulated polymorphic populations

Reinforcement speciation is the process whereby selection against hybrids drives the evolution of enhanced pre-mating reproductive isolation. Work has focused on divergent mating preferences (assortative mating) but pre-mating isolation can also arise via various migration modification behaviours, such as divergent habitat preferences. The relative importance of these two different mechanisms of reinforcement remains unclear. A recent theoretical model (Yukilevich-True model) found that relative fixation probabilities between these mechanisms can vary. Additionally, natural populations of Timema cristinae walking-sticks exhibit variation (polymorphism) in both mechanisms, generating questions about the patterns expected for allele frequencies prior to fixation, during the early stages of the speciation process. In the present study, we report: (1) new analyses examining the correlation between fixation probabilities for assortative mating and migration modification in the Yukilevich-True model; (2) novel simulations examining allele frequencies in polymorphic populations; and (3) empirical patterns of reinforcement in T. cristinae in the context of theoretical predictions. Simulations of both types yielded congruent results, revealing that the outcome of reinforcement was dependent on the strength of selection. Under weak selection, reinforcement by either mechanism is unlikely. Under intermediate selection, the conditions favoring the rise and fixation of one mechanism favored the rise and fixation of the other. However, assortative mating evolved somewhat more readily than migration modification. Populations of T. cristinae, which experience such intermediate selection, supported these predictions. Under strong selection, the evolution of migration modification generally interfered with the evolution of assortative mating by decreasing migration between populations, thereby reducing selection for assortative mating. Congruence of the results for allele frequencies versus fixation probabilities suggests that similar patterns of reinforcement are expected during different stages of the speciation process

Isolation, Characterization, and Synthesis of Cuticular Hydrocarbon Natural Products from Drosophila athabasca, A Species of Evolutionary Interest

Drosophila athabasca, a species complex native to North America, provides a unique opportunity to study nascent speciation arising from sexual isolation. Some have suggested that cuticular hydrocarbons (CHCs) influence the sexual selection process. Extensive analyses have resulted in complex understandings of CHC involvement in insect mate preference, with minimal work focusing on D. athabasca. The goal of this study is to identify, synthesize and measure biologically relevant quantities of CHCs present in this species complex. Gas chromatography – mass spectrometry (GC-MS) from several isofemale lines of D. athabasca allows for characterization of contributing compounds including saturated, unsaturated, and branched alkanes, fatty acids, acetates, and esters. Identification of these compounds using characteristic fragmentation patterns allowed for confirmation by synthetic standards. To date, over 100 CHCs have been characterized in D. athabasca using these analytical and organic methods. An overview of the analysis techniques and future direction will be presented.https://digitalworks.union.edu/steinmetz_posters/1009/thumbnail.jp

Incompatibility and Competitive Exclusion of Genomic Segments between Sibling Drosophila Species

The extent and nature of genetic incompatibilities between incipient races and sibling species is of fundamental importance to our view of speciation. However, with the exception of hybrid inviability and sterility factors, little is known about the extent of other, more subtle genetic incompatibilities between incipient species. Here we experimentally demonstrate the prevalence of such genetic incompatibilities between two young allopatric sibling species, Drosophila simulans and D. sechellia. Our experiments took advantage of 12 introgression lines that carried random introgressed D. sechellia segments in different parts of the D. simulans genome. First, we found that these introgression lines did not show any measurable sterility or inviability effects. To study if these sechellia introgressions in a simulans background contained other fitness consequences, we competed and genetically tracked the marked alleles within each introgression against the wild-type alleles for 20 generations. Strikingly, all marked D. sechellia introgression alleles rapidly decreased in frequency in only 6 to 7 generations. We then developed computer simulations to model our competition results. These simulations indicated that selection against D. sechellia introgression alleles was high (average s = 0.43) and that the marker alleles and the incompatible alleles did not separate in 78% of the introgressions. The latter result likely implies that most introgressions contain multiple genetic incompatibilities. Thus, this study reveals that, even at early stages of speciation, many parts of the genome diverge to a point where introducing foreign elements has detrimental fitness consequences, but which cannot be seen using standard sterility and inviability assays

The causes of epistasis in genetic networks

[EN] Epistasis refers to the nonadditive interactions between genes in determining phenotypes. Considerable efforts have shown that, even for a given organism, epistasis may vary both in intensity and sign. Recent comparative studies supported that the overall sign of epistasis switches from positive to negative as the complexity of an organism increases, and it has been hypothesized that this change shall be a consequence of the underlying gene network properties. Why should this be the case? What characteristics of genetic networks determine the sign of epistasis? Here we show, by evolving genetic networks that differ in their complexity and robustness against perturbations but that perform the same tasks, that robustness increased with complexity and that epistasis was positive for small nonrobust networks but negative for large robust ones. Our results indicate that robustness and negative epistasis emerge as a consequence of the existence of redundant elements in regulatory structures of genetic networks and that the correlation between complexity and epistasis is a byproduct of such redundancy, allowing for the decoupling of epistasis from the underlying network complexity.We thank J. Carrera, J. A. G. M. de Visser, M. A. Fares, and S. Valverde for discussions and two anonymous reviewers for insightful suggestions. This work was supported by the Spanish Ministry of Science and Innovation grant BFU2009-06993 (SFE), the Generalitat Valenciana grant PROMETEO2010/019 (SFE), the Human Frontiers Science Program grant RGP12/2008 (SFE and RVS), and the Santa Fe Institute.Macia, J.; Sole, RV.; Elena Fito, SF. (2012). The causes of epistasis in genetic networks. Evolution. 66(2):586-596. https://doi.org/10.1111/j.1558-5646.2011.01451.xS58659666

The past and future of experimental speciation

Speciation is the result of evolutionary processes that generate barriers to gene flow between populations, facilitating reproductive isolation. Speciation is typically studied via theoretical models and “snap-shot” tests in natural populations. Experimental speciation enables real-time direct tests of speciation theory and has been long-touted as a critical complement to other approaches. We argue that, despite its promise to elucidate the evolution of reproductive isolation, experimental speciation has been underutilised and lags behind other contributions to speciation research. We review recent experiments and outline a framework for how experimental speciation can be implemented to address current outstanding questions that are otherwise challenging to answer. Greater uptake of this approach is necessary to rapidly advance understanding of speciation

Are assortative mating and genital divergence driven by reinforcement?

The evolution of assortative mating is a key part of the speciation process. Stronger assortment, or greater divergence in mating traits, between species pairs with overlapping ranges is commonly observed, but possible causes of this pattern of reproductive character displacement are difficult to distinguish. We use a multidisciplinary approach to provide a rare example where it is possible to distinguish among hypotheses concerning the evolution of reproductive character displacement. We build on an earlier comparative analysis that illustrated a strong pattern of greater divergence in penis form between pairs of sister species with overlapping ranges than between allopatric sister-species pairs, in a large clade of marine gastropods (Littorinidae). We investigate both assortative mating and divergence in male genitalia in one of the sister-species pairs, discriminating among three contrasting processes each of which can generate a pattern of reproductive character displacement: reinforcement, reproductive interference and the Templeton effect. We demonstrate reproductive character displacement in assortative mating, but not in genital form between this pair of sister species and use demographic models to distinguish among the different processes. Our results support a model with no gene flow since secondary contact and thus favor reproductive interference as the cause of reproductive character displacement for mate choice, rather than reinforcement. High gene flow within species argues against the Templeton effect. Secondary contact appears to have had little impact on genital divergence

Genetics of Dispersal

Dispersal is a process of central importance for the ecological and evolutionary dynamics of populations and communities, because of its diverse consequences for gene flow and demography. It is subject to evolutionary change, which begs the question, what is the genetic basis of this potentially complex trait? To address this question, we (i) review the empirical literature on the genetic basis of dispersal, (ii) explore how theoretical investigations of the evolution of dispersal have represented the genetics of dispersal, and (iii) discuss how the genetic basis of dispersal influences theoretical predictions of the evolution of dispersal and potential consequences. Dispersal has a detectable genetic basis in many organisms, from bacteria to plants and animals. Generally, there is evidence for significant genetic variation for dispersal or dispersal-related phenotypes or evidence for the micro-evolution of dispersal in natural populations. Dispersal is typically the outcome of several interacting traits, and this complexity is reflected in its genetic architecture: while some genes of moderate to large effect can influence certain aspects of dispersal, dispersal traits are typically polygenic. Correlations among dispersal traits as well as between dispersal traits and other traits under selection are common, and the genetic basis of dispersal can be highly environment-dependent. By contrast, models have historically considered a highly simplified genetic architecture of dispersal. It is only recently that models have started to consider multiple loci influencing dispersal, as well as non-additive effects such as dominance and epistasis, showing that the genetic basis of dispersal can influence evolutionary rates and outcomes, especially under non-equilibrium conditions. For example, the number of loci controlling dispersal can influence projected rates of dispersal evolution during range shifts and corresponding demographic impacts. Incorporating more realism in the genetic architecture of dispersal is thus necessary to enable models to move beyond the purely theoretical towards making more useful predictions of evolutionary and ecological dynamics under current and future environmental conditions. To inform these advances, empirical studies need to answer outstanding questions concerning whether specific genes underlie dispersal variation, the genetic architecture of context-dependent dispersal phenotypes and behaviours, and correlations among dispersal and other traits.Peer reviewe

Divergence in female damselfly sensory structures is consistent with a species recognition function but shows no evidence of reproductive character displacement

Males and females transmit and receive signals prior to mating that convey information such as sex, species identity, or individual condition. In some animals, tactile signals relayed during physical contact between males and females before and during mating appear to be important for mate choice or reproductive isolation. This is common among odonates, when a male grasps a female's thorax with his terminal appendages prior to copulation, and the female subsequently controls whether copulation occurs by bending her abdomen to complete intromission. It has been hypothesized that mechanosensory sensilla on the female thoracic plates mediate mating decisions, but is has been difficult to test this idea. Here, we use North American damselflies in the genus Enallagma (Odonata: Coenagrionidae) to test the hypothesis that variation in female sensilla traits is important for species recognition. Enallagma anna and E. carunculatum hybridize in nature, but experience strong reproductive isolation as a consequence of divergence in male terminal appendage morphology. We quantified several mechanosensory sensilla phenotypes on the female thorax among multiple populations of both species and compared divergence in these traits in sympatry versus allopatry. Although these species differed in features of sensilla distribution within the thoracic plates, we found no strong evidence of reproductive character displacement among the sensilla traits we measured in regions of sympatry. Our results suggest that species‐specific placement of female mechanoreceptors may be sufficient for species recognition, although other female sensory phenotypes might have diverged in sympatry to reduce interspecific hybridization.This work was supported by funds from the University of Oklahoma. We are grateful to assistance with publication costs from OU's University Libraries Open Access fund.Ye

The effects of purifying selection on patterns of genetic differentiation between Drosophila melanogaster populations.

Using the data provided by the Drosophila Population Genomics Project, we investigate factors that affect the genetic differentiation between Rwandan and French populations of D. melanogaster. By examining within-population polymorphisms, we show that sites in long introns (especially those >2000 bp) have significantly lower π (nucleotide diversity) and more low-frequency variants (as measured by Tajima's D, minor allele frequencies, and prevalence of variants that are private to one of the two populations) than short introns, suggesting a positive relationship between intron length and selective constraint. A similar analysis of protein-coding polymorphisms shows that 0-fold (degenerate) sites in more conserved genes are under stronger purifying selection than those in less conserved genes. There is limited evidence that selection on codon bias has an effect on differentiation (as measured by FST) at 4-fold (degenerate) sites, and 4-fold sites and sites in 8-30 bp of short introns ⩽65 bp have comparable FST values. Consistent with the expected effect of purifying selection, sites in long introns and 0-fold sites in conserved genes are less differentiated than those in short introns and less conserved genes, respectively. Genes in non-crossover regions (for example, the fourth chromosome) have very high FST values at both 0-fold and 4-fold degenerate sites, which is probably because of the large reduction in within-population diversity caused by tight linkage between many selected sites. Our analyses also reveal subtle statistical properties of FST, which arise when information from multiple single nucleotide polymorphisms is combined and can lead to the masking of important signals of selection