scholarly journals Pervasive genetic associations between traits causing reproductive isolation in Heliconius butterflies

2010 ◽  
Vol 278 (1705) ◽  
pp. 511-518 ◽  
Author(s):  
Richard M. Merrill ◽  
Bas Van Schooten ◽  
Janet A. Scott ◽  
Chris D. Jiggins

Ecological speciation proceeds through the accumulation of divergent traits that contribute to reproductive isolation, but in the face of gene flow traits that characterize incipient species may become disassociated through recombination. Heliconius butterflies are well known for bright mimetic warning patterns that are also used in mate recognition and cause both pre- and post-mating isolation between divergent taxa. Sympatric sister taxa representing the final stages of speciation, such as Heliconius cydno and Heliconius melpomene , also differ in ecology and hybrid fertility. We examine mate preference and sterility among offspring of crosses between these species and demonstrate the clustering of Mendelian colour pattern loci and behavioural loci that contribute to reproductive isolation. In particular, male preference for red patterns is associated with the locus responsible for the red forewing band. Two further colour pattern loci are associated, respectively, with female mating outcome and hybrid sterility. This genetic architecture in which ‘speciation genes’ are clustered in the genome can facilitate two controversial models of speciation, namely divergence in the face of gene flow and hybrid speciation.

2019 ◽  
Author(s):  
M.F. González-Rojas ◽  
K. Darragh ◽  
J Robles ◽  
M. Linares ◽  
S Schulz ◽  
...  

ABSTRACTColour pattern has been long recognised as the trait that drives mate recognition betweenHeliconiusspecies that are phylogenetically close. However, when this cue is compromised such as in cases of mimetic, sympatric and closely related species, alternative mating signals must evolve to ensure reproductive isolation and species integrity. The closely related speciesHeliconius melpomene malletiandH. timareta florencia, occur in the same geographic region and despite being co-mimics they display strong reproductive isolation. In order to test which cues differ between species, and therefore potentially contribute to reproductive isolation, we quantified differences in wing phenotype and male chemical profile. As expected, wing colour pattern was indistinguishable between the two species while the chemical profile of their male sex pheromones showed marked differences. We then conducted behavioural experiments to study the importance of these signals in mate recognition by females. In agreement with our previous results, we found that pheromones and not wing colour pattern drive the preference of females by conspecific males. In addition, experiments with hybrid males and females suggested an important genetic component for both pheromone production and preference. Altogether, these results suggest that pheromones are the major reproductive barrier opposing gene flow between these two sister and co-mimic species.


2008 ◽  
Vol 363 (1506) ◽  
pp. 3047-3054 ◽  
Author(s):  
Chris D Jiggins ◽  
Camilo Salazar ◽  
Mauricio Linares ◽  
Jesus Mavarez

Homoploid hybrid speciation (HHS) is the establishment of a novel species through introgressive hybridization without a change in chromosome number. We discuss different routes by which this might occur and propose a novel term, ‘hybrid trait speciation’, which combines the idea that hybridization can generate adaptive novelty with the ‘magic trait’ model of ecological speciation. Heliconius butterflies contain many putative examples of hybrid colour patterns, but only recently has the HHS hypothesis been tested explicitly in this group. Molecular data has shown evidence for gene flow between many distinct species. Furthermore, the colour pattern of Heliconius heurippa can be recreated in laboratory crosses between Heliconius melpomene and Heliconius cydno and, crucially, plays a role in assortative mating between the three species. Nonetheless, although the genome of H. heurippa shows evidence for hybridization, it is not a mosaic of the two parental species. Instead, ongoing hybridization has likely blurred any signal of the original speciation event. We argue that where hybridization leads to novel adaptive traits that also cause reproductive isolation, it is likely to trigger speciation.


2017 ◽  
Vol 284 (1856) ◽  
pp. 20170335 ◽  
Author(s):  
C. Mérot ◽  
C. Salazar ◽  
R. M. Merrill ◽  
C. D. Jiggins ◽  
M. Joron

The process by which species evolve can be illuminated by investigating barriers that limit gene flow between taxa. Recent radiations, such as Heliconius butterflies, offer the opportunity to compare isolation between pairs of taxa at different stages of ecological, geographical, and phylogenetic divergence. Here, we report a comparative analysis of existing and novel data in order to quantify the strength and direction of isolating barriers within a well-studied clade of Heliconius . Our results highlight that increased divergence is associated with the accumulation of stronger and more numerous barriers to gene flow. Wing pattern is both under natural selection for Müllerian mimicry and involved in mate choice, and therefore underlies several isolating barriers. However, pairs which share a similar wing pattern also display strong reproductive isolation mediated by traits other than wing pattern. This suggests that, while wing pattern is a key factor for early stages of divergence, it may become facultative at later stages of divergence. Additional factors including habitat partitioning, hybrid sterility, and chemically mediated mate choice are associated with complete speciation. Therefore, although most previous work has emphasized the role of wing pattern, our comparative results highlight that speciation is a multi-dimensional process, whose completion is stabilized by many factors.


2020 ◽  
Vol 287 (1926) ◽  
pp. 20200587 ◽  
Author(s):  
M. F. González-Rojas ◽  
K. Darragh ◽  
J. Robles ◽  
M. Linares ◽  
S. Schulz ◽  
...  

Colour pattern is the main trait that drives mate recognition between Heliconius species that are phylogenetically close. However, when this cue is compromised such as in cases of mimetic, sympatric and closely related species, alternative mating signals must evolve to ensure reproductive isolation and species integrity. The closely related species Heliconius melpomene malleti and H. timareta florencia occur in the same geographical region, and despite being co-mimics, they display strong reproductive isolation. In order to test which cues differ between species, and potentially contribute to reproductive isolation, we quantified differences in the wing phenotype and the male chemical profile. As expected, the wing colour pattern was indistinguishable between the two species, while the chemical profile of the androconial and genital males' extracts showed marked differences. We then conducted behavioural experiments to study the importance of these signals in mate recognition by females. In agreement with our previous results, we found that chemical blends and not wing colour pattern drive the preference of females for conspecific males . Also, experiments with hybrid males and females suggested an important genetic component for both chemical production and preference. Altogether, these results suggest that chemicals are the major reproductive barrier opposing gene flow between these two sister and co-mimic species.


Evolution ◽  
2013 ◽  
Vol 68 (4) ◽  
pp. 935-949 ◽  
Author(s):  
Roger K. Butlin ◽  
Maria Saura ◽  
Grégory Charrier ◽  
Benjamin Jackson ◽  
Carl André ◽  
...  

2021 ◽  
Author(s):  
Karenleigh A. Overmann ◽  
Frederick L. Coolidge

The present paper examined the assumption of strong reproductive isolation (RI) between Homo neanderthalensis and Homo sapiens, as well as the question of what form it might have taken, using insights from the parallel case of chimpanzee–bonobo hybridization. RI from hybrid sterility or inviability was thought unlikely based on the short separation-to-introgression timeline. The forms of RI that typically develop in primates have relatively short timelines (especially for partial implementation); they generally preclude mating or influence hybrid survival and reproduction in certain contexts, and they have the potential to skew introgression directionality. These RI barriers are also consistent with some interpretations of the archaeological and fossil records, especially when behavioral, cognitive, morphological, and genetic differences between the two human species are taken into consideration. Differences potentially influencing patterns of survival and reproduction include interspecies violence, Neandertal xenophobia, provisioning behavior, and ontogenetic, morphological, and behavioral differences affecting matters such as kin and mate recognition, infanticide, and sexual selection. These factors may have skewed the occurrence of interbreeding or the survival and reproduction of hybrids in a way that might at least partially explain the pattern of introgression.


2020 ◽  
Vol 12 (2) ◽  
pp. 41
Author(s):  
Roshni Singh ◽  
Bashisth Narayan Singh

There are several barriers to preclude the gene flow between diverging populations. On the basis of their temporal nature, these can be broadly categorized into two forms: pre- and post-zygotic. Post-zygotic reproductive isolation can manifest in the form of reductions in hybrid fertility. Keeping this fact in view, in the present study, we studied sterility in hybrids of D. ananassae and D. pallidosa. Surprisingly a distinguishable pattern of infertility was found in the hybrids. This pattern, referred to as Haldane’s rule, is often observed in hybrids of recently diverged populations or species. Reduction in the fertility of hybrids provides the clue of incipient kind of post-zygotic reproductive isolation in these two sibling species. This is the first report of hybrid sterility in this species pair. However, hybrid sterility is not very prominent especially when compared to that of other species pairs with the similar divergence time. Thus, on the basis of our results, we conclude that either sexual isolation between these sibling species is sufficient and does not require the aid of post-zygotic isolation to preclude gene flow or rate of divergence between D. ananassae and D. pallidosa is very slow in comparison to other species pair or even races of some species.


2017 ◽  
Author(s):  
C. Mérot ◽  
C. Salazar ◽  
R. M. Merrill ◽  
C. Jiggins ◽  
M. Joron

AbstractThe process by which species evolve can be illuminated by investigating barriers that limit gene flow between taxa. Recent radiations, such as Heliconius butterflies, offer the opportunity to compare isolation between pairs of taxa at different stages of ecological, geographic and phylogenetic divergence. We carry out a comparative analysis of existing and novel data in order to quantify the strength and direction of isolating barriers within a well-studied clade of Heliconius. Our results highlight that increased divergence is associated with the accumulation of stronger and more numerous barriers to gene flow. Wing pattern is both under natural selection for Müllerian mimicry and involved in mate choice, and therefore underlies several isolating barriers. However, pairs which share a similar wing pattern, also display strong reproductive isolation mediated by traits other than wing pattern. This suggests that, while wing pattern is a key factor for early stages of divergence, it is not essential at a higher level. Additional factors including habitat isolation, hybrid sterility and chemically-mediated mate choice are associated with complete speciation. Therefore, although most previous work has emphasised the role of wing pattern, our comparative results highlight that speciation is a multidimensional process, whose completion is stabilized by many factors.


2017 ◽  
Author(s):  
David A. Turissini ◽  
Joseph A. McGirr ◽  
Sonali S. Patel ◽  
Jean R. David ◽  
Daniel R. Matute

ABSTRACTReproductive isolation (RI) is an intrinsic aspect of species, as described in the Biological Species Concept. For that reason, the identification of the precise traits and mechanisms of RI, and the rates at which they evolve, is crucial to understanding how species originate and persist. Nonetheless, precise measurements of the magnitude of reproductive isolation are rare. Previous work has measured the rates of evolution of prezygotic and postzygotic barriers to gene flow, yet no systematic analysis has carried out the study of the rates of evolution of postmating-prezygotic (PMPZ) barriers. We systematically measured the magnitude of two barriers to gene flow that act after mating occurs but before zygotic fertilization and also measured a premating (female mating rate in nonchoice experiments) and two postzygotic barriers (hybrid inviability and hybrid sterility) for all pairwise crosses of species within the Drosophila melanogaster subgroup. Our results indicate that PMPZ isolation evolves faster than hybrid inviability but slower than premating isolation. We also describe seven new interspecific hybrids in the group. Our findings open up a large repertoire of tools that will enable researchers to manipulate hybrids and explore the genetic basis of interspecific differentiation, reproductive isolation, and speciation.


2015 ◽  
Author(s):  
Simon Henry Martin ◽  
Anders Eriksson ◽  
Krzysztof M. Kozak ◽  
Andrea Manica ◽  
Chris D. Jiggins

Documenting the full extent of gene flow during speciation poses a challenge, as species ranges change over time and current rates of hybridisation might not reflect historical trends. Theoretical work has emphasized the potential for speciation in the face of ongoing hybridisation, and the genetic mechanisms that might facilitate this process. However, elucidating how the rate of gene flow between species may have changed over time has proved difficult. Here we use Approximate Bayesian Computation (ABC) to fit a model of speciation between the Neotropical butterflies Heliconius melpomene and Heliconius cydno. These species are ecologically divergent, rarely hybridize and display female hybrid sterility. Nevertheless, previous genomic studies suggests pervasive gene flow between them, extending deep into their past, and potentially throughout the speciation process. By modelling the rates of gene flow during early and later stages of speciation, we find that these species have been hybridising for hundreds of thousands of years, but have not done so continuously since their initial divergence. Instead, it appears that gene flow was rare or absent for as long as a million years in the early stages of speciation. Therefore, by dissecting the timing of gene flow between these species, we are able to reject a scenario of purely sympatric speciation in the face of continuous gene flow. We suggest that the period of minimal contact early in speciation may have allowed for the accumulation of genomic changes that later enabled these species to remain distinct despite a dramatic increase in the rate of hybridisation.


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