Background: The independent evolution of sympatric species pairs of threespine sticklebacks has provided a natural system to explore how divergent ecologies shape mating preferences. Research has shown that both limnetic and benthic females discriminate against heterospecific males, but not against populations of the same species from different lakes, at least when visual cues are available (Rundle et al., 2000). It is known that olfaction is used in species dis- crimination by benthic but not limnetic sticklebacks in one of the species pairs (Rafferty and Boughman, 2006), but differences across populations are unknown. Hypotheses: Females from benthic habitats make use of olfactory cues to distinguish between species but not lakes of potential mates. Limnetic females will not show preferences for males of different species or lakes when limited to only olfactory cues. Organisms: Benthic and limnetic populations of threespine stickleback (Gasterosteus aculeatus) from Paxton and Priest Lakes, British Columbia. Methods: We exposed gravid females from each population to chemical stimuli from nesting males in a Y-maze, and recorded which stimulus a female chose and how much time was taken to make a decision. Results: We did not find significant differences between female populations in the preference for conspecific over heterospecific male odours. There was also no preference for odours of males from the same or a different lake. In all populations of females, the preference for male odours of different lakes differed between the two species of male odours: benthic male odours from a different lake were selected over limnetic male odours. The amount of time taken to make a decision differed between female populations, but only when benthic females ultimately chose a limnetic male odour over a benthic one. Conclusions: The preference for conspecific over heterospecific odours, although not strong, may still contribute to reproductive isolation in sympatric sticklebacks, particularly through interactions with other senses and environmental properties.
more »
« less
Conflict over fertilization underlies the transient evolution of reinforcement
When two species meet in secondary contact, the production of low fitness hybrids may be prevented by the adaptive evolution of increased prezygotic isolation, a process known as reinforcement. Theoretical challenges to the evolution of reinforcement are generally cast as a coordination problem, i.e., “how can statistical associations between traits and preferences be maintained in the face of recombination?” However, the evolution of reinforcement also poses a potential conflict between mates. For example, the opportunity costs to hybridization may differ between the sexes or species. This is particularly likely for reinforcement based on postmating prezygotic (PMPZ) incompatibilities, as the ability to fertilize both conspecific and heterospecific eggs is beneficial to male gametes, but heterospecific mating may incur a cost for female gametes. We develop a population genetic model of interspecific conflict over reinforcement inspired by “gametophytic factors”, which act as PMPZ barriers among Zea mays subspecies. We demonstrate that this conflict results in the transient evolution of reinforcement—after females adaptively evolve to reject gametes lacking a signal common in conspecific gametes, this gamete signal adaptively introgresses into the other population. Ultimately, the male gamete signal fixes in both species, and isolation returns to pre-reinforcement levels. We interpret geographic patterns of isolation among Z . mays subspecies considering these findings and suggest when and how this conflict can be resolved. Our results suggest that sexual conflict over fertilization may pose an understudied obstacle to the evolution of reinforcement.
more »
« less
- Award ID(s):
- 1753632
- PAR ID:
- 10390413
- Editor(s):
- Jennions, Michael D.
- Date Published:
- Journal Name:
- PLOS Biology
- Volume:
- 20
- Issue:
- 10
- ISSN:
- 1545-7885
- Page Range / eLocation ID:
- e3001814
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Many traits important for reproductive isolation are environmentally responsive. However, most studies examining reproductive isolation do not explicitly take into consideration environmental variation. Temperature can have a particularly large effect on reproductive behaviours, especially in ectotherms. Here, we tested whether temperature affects the degree of reproductive isolation between the upland chorus frog, Pseudacris feriarum, and its congener Pseudacris nigrita. These two species engage in costly hybridization in nature, leading to reinforcement of male signals and female preferences in sympatry. However, male advertisement calls vary with temperature such that the difference between the advertisement calls of the two species is narrower at cold temperatures than at warm temperatures. To examine the effect of temperature on reproductive isolation in this system, we performed six binary choice preference trials using sympatric female P. feriarum. In these experiments, we acclimated females to either warm (20 °C) or cool (10 °C) temperatures and gave them a choice between heterospecific and conspecific advertisement calls appropriate for the temperature. We also conducted experiments where we gave females a choice between more similar stimuli at warm temperatures to test whether females have narrower preferences at cold temperatures. We found that females always had a significant preference for the conspecific advertisement call, regardless of temperature or signal similarity. However, females took twice as long to make a choice in suboptimal conditions. This time delay may lead to increased risk of hybridization, despite females’ ability to discriminate between calls. Our results highlight the importance of considering environmental context when examining traits involved in reproductive isolation.more » « less
-
Abstract The establishment of reproductive isolation between species via gametic incompatibility initially requires within-species variation in reproductive compatibility. We investigate how within-species variation in sperm and egg recognition proteins, potentially generated via sexual conflict, influences reproductive isolation between two partially sympatric sea urchin species; the North American west coast Mesocentrotus franciscanus and the circumpolar Strongylocentrotus droebachiensis. Barriers to hybridization are stronger when eggs are given a choice of conspecific versus heterospecific sperm and the variation in hybridization among crosses can be explained by whether the sperm or egg protein variant is ancestral or derived. Derived proteins can be recognized as different and prevent hybridization. Examination of the allele frequencies of these proteins in M. franciscanus in and out of sympatry with S. droebachiensis along the west coast of North America reveals evidence of reinforcement selection and reproductive character displacement in eggs but not sperm, which likely reflects the differential cost of hybridization for males and females.more » « less
-
Abstract The role of hybridization as a formative process in evolution has received much attention in the past few decades. A particularly fascinating outcome of hybrid speciation is the formation of asexual hybrid species. The Amazon molly (Poecilia formosa) is such a hybrid and originated from aP. mexicanamother and aP. latipinnafather. Consequently, a heterospecific mating must have occurred leading to the Amazon molly, indicating a breakdown of any potential prezygotic isolation between parental species. Here we studied the female mate preferences of extantP. mexicanaandP. latipinnafrom several populations using standard binary choice tests with males of both sexual species that were matched for size.Poecilia mexicanaandP. latipinnacan be crossed in the lab, however, the offspring are not asexual, but sexual F1s. In our study, we generated F1s and tested their mating preferences with sexual males of bothP. mexicanaandP. latipinnaagainst F1males. Overall, our results show that in extantP. mexicanaandP. latipinnano female preference for conspecific males was detectable. Consequently, heterospecific matings are possible and not hindered by any apparent behavioral prezygotic isolation. If female preferences in these species were comparable around the time the Amazon molly originated as a hybrid species ca. 100,000 years ago, matings leading to hybrids would be very likely. F1females also have no discernable mating preferences for either sexual males or F1males. Such lack of prezygotic behavioral isolation could potentially lead to F2individuals, backcrosses, and introgression.more » « less
-
Mating with another species is often maladaptive because it generally results in no or low-fitness offspring. When hybridization is sufficiently costly, individuals should avoid mating with heterospecifics even if it reduces their ability to mate with high-quality conspecifics that resemble heterospecifics. Here, we used spadefoot toads, Spea multiplicata, to evaluate whether females alter their preferences for conspecific male sexual signals (call rate) depending on heterospecific presence. When presented with conspecific signals against a background including both conspecific and heterospecific signals, females preferred male traits that were most dissimilar to heterospecifics—even though these signals are potentially associated with lower-quality mates. However, when these same females were presented with a background that included only conspecific signals, some females switched their preferences, choosing conspecific signals that were exaggerated and indicative of high-quality conspecific mates. Because only some females switched their preferences between these two chorus treatments, there was no population-level preference for exaggerated conspecific male signals in the absence of heterospecifics. These results show that hybridization risk can alter patterns of mate choice and, consequently, sexual selection on male signals. Moreover, they emphasize that the strength and expression of reproductive barriers between species (such as mate choice) can be context-dependent.more » « less
An official website of the United States government

