Experimental evolution with an insect model reveals that male homosexual behaviour occurs due to inaccurate mate choice

Sales, Kris; Trent, Thomas; Gardner, Jessie; Lumley, Alyson J.; Vasudeva, Ramakrishnan; Michalczyk, Łukasz; Martin, Oliver Y.; Gage, Matthew J. G.

doi:10.1016/j.anbehav.2018.03.004

Cited by 30 publications

(33 citation statements)

References 50 publications

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“…To assess impacts within the relevant context of sperm competition, we measured how heatwave conditions influenced a male’s subsequent ability to win fertilisations within females that had previously been mated to untreated, marker males. Males were sexed as pupae, and then isolated from eclosion until experimental mating to standardise and prevent any confounds from uncontrolled same-sex behaviour activity 69 . Treatment males were exposed to 5 days at 30 °C (controls) or 42 °C (heatwaves), followed by 24 h at 30 °C.…”

Section: Methodsmentioning

confidence: 99%

“…Males sexed as pupae were individually isolated before their mating behaviour assay to prevent any same-sex activity and to standardise all individuals prior to each trial 64 , 69 . At adult maturity, males were exposed for 5-day treatments at 30 °C ( n = 25), 39 °C ( n = 24), 40 °C ( n = 21), 41 °C ( n = 24) or 42 °C ( n = 14), followed by 24 h at 30 °C (Supplementary Figure 4c ).…”

Section: Methodsmentioning

confidence: 99%

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Experimental heatwaves compromise sperm function and cause transgenerational damage in a model insect

et al. 2018

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Climate change is affecting biodiversity, but proximate drivers remain poorly understood. Here, we examine how experimental heatwaves impact on reproduction in an insect system. Male sensitivity to heat is recognised in endotherms, but ectotherms have received limited attention, despite comprising most of biodiversity and being more influenced by temperature variation. Using a flour beetle model system, we find that heatwave conditions (5 to 7 °C above optimum for 5 days) damaged male, but not female, reproduction. Heatwaves reduce male fertility and sperm competitiveness, and successive heatwaves almost sterilise males. Heatwaves reduce sperm production, viability, and migration through the female. Inseminated sperm in female storage are also damaged by heatwaves. Finally, we discover transgenerational impacts, with reduced reproductive potential and lifespan of offspring when fathered by males, or sperm, that had experienced heatwaves. This male reproductive damage under heatwave conditions provides one potential driver behind biodiversity declines and contractions through global warming.

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Experimental heatwaves compromise sperm function and cause transgenerational damage in a model insect

et al. 2018

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“…Natural mating disruption (high rates of FMF on crowded host plants) can arise due to: (1) males being unable to discriminate receptive females from conspecific males or non receptive females (Richerson et al, 1976;Takeuchi, 2017;Sales et al, 2018), (2) passive olfactory signals of post reproductive conspecifics interfering with mate location (Gwynne & Lorch, 2013;Rhainds, 2018), or (3) adsorption of pheromone onto the foliage of host plants (Noldus et al, 1991). Testing these hypotheses requires small-scale mapping of female mating probability among georeferenced plants (van Wijk et al, 2017;Muniz et al, 2018;Sciarretta et al, 2018).…”

Section: Signal Interference and Natural Mating Disruptionmentioning

confidence: 99%

Ecology of female mating failure/lifelong virginity: a review of causal mechanisms in insects and arachnids

Rhainds

2019

Entomologia Exp Applicata

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Sexual reproduction implies binary outcomes of competitive interactions for access to male gametes: lifelong virgin females with null fitness vs. mated females with variable (generally nonzero) fitness. Female mating failure has long remained a dormant concept in sexual selection theory in part because it is acutely maladaptive (lifelong virgins that do not reproduce are strongly selected against) and also due to widespread acceptance of the Bateman–Trivers paradigm (anisogamy and correlated sex roles). Based on recent scientific output on lifelong virginity across multiple taxonomic groups in insects (Coleoptera, Diptera, Hemiptera, Lepidoptera, Odonata, Orthoptera, Strepsiptera), female mating failure has become a mainstay of sexual selection over the last decade. Lifelong virginity and senescence (death) are intertwined processes; old virgin females compensate for increased risk of lifelong virginity by becoming less choosy and increasing investment in mating‐related activities. Low rates of female lifelong virginity (<5%) in most natural populations of insects indicate that sex generally ‘works’ due to selective pressures acting on both males and females to enhance lifetime fitness. Mating failures are most common in insects with female flightlessness; these pressures may lead in evolutionary time to transitionary pathways from sexual reproduction to parthenogenesis. Female mating probability is affected by nonlinear density‐dependent processes dependent upon the scale of observation (mate‐encounter Allee effect at large spatial scales, mating interferences between females at small scales). Mate choice and sex role reversal (females being the active sexual partner) are ubiquitous in insects and arachnids with significant paternal investment, but consequences in terms of female lifelong virginity remain unknown. Logistically, conceptual development of female mating failure in insects is most limited by the lack of broadly applicable methods to assess rates of lifetime virginity among flighted females.

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“…SSB is often considered a result of mistaken identity [39][40][41] , as is suggested to account for about 80% of reported cases in arthropods 3 . Our model provides an evolutionary perspective on this mistaken identity hypothesis, suggesting that poor sex identification could actually occur as an optimal strategy.…”

Section: Discussionmentioning

confidence: 99%

Same-sex sexual behavior and selection for indiscriminate mating

Lerch

Servedio

2020

Preprint

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The widespread presence of same-sex sexual behavior (SSB) has long been thought to pose an evolutionary conundrum1-3, as participants in SSB suffer the cost of failing to reproduce after expending the time and energy to find a mate. The potential for SSB to occur as part of an optimal strategy has received almost no attention, although indiscriminate sexual behavior may be the ancestral mode of sexual reproduction4. Here, we build a simple model of sexual reproduction and create a theoretical framework for the evolution of indiscriminate sexual behavior. We provide strong support for the hypothesis that SSB is likely maintained by selection for indiscriminate sexual behavior, by showing that indiscriminate mating is the optimal strategy under a wide range of conditions. Further, our model suggests that the conditions that most strongly favor indiscriminate mating were likely present at the origin of sexual behavior. These findings have implications not only for the evolutionary origins of SSB, but also for the evolution of discriminate sexual behavior across the animal kingdom.

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Experimental evolution with an insect model reveals that male homosexual behaviour occurs due to inaccurate mate choice

Cited by 30 publications

References 50 publications

Experimental heatwaves compromise sperm function and cause transgenerational damage in a model insect

Experimental heatwaves compromise sperm function and cause transgenerational damage in a model insect

Ecology of female mating failure/lifelong virginity: a review of causal mechanisms in insects and arachnids

Same-sex sexual behavior and selection for indiscriminate mating

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