Tough choices in love: wait to mate or settle for Mr. Right-now.

Blog written by Kerianne Wilson. Read the full paper here.

Which male a female decides to mate with can have profound effects on how likely her genes are to remain in the population in future generations. From an evolutionary standpoint, females should try to mate with a male that allows her to produce the most offspring with the best genes possible. However, females may be faced with a situation in which they are unable to find a high-quality mate and must decide whether to postpone reproduction to search for a better male or settle for the male at hand. While waiting to find a better mate may seem like the best choice, there are usually costs involved in waiting to invest in reproduction.

A corner stone of life history theory is the trade-off between allocating limited resources (i.e. nutrients) to survival versus reproduction. This means that if a female invests more in her own survival, she may not have as many resources to shunt towards producing offspring. Thus, if only low-quality males are available when females are ready to reproduce, those that postpone reproduction in hopes of finding a better mate may produce fewer offspring than females that settle for an available, low-quality male. An additional complication to this choice is the possibility that males of different qualities may attempt to manipulate how a female allocates resources to suit the male’s own interests. This form of sexual conflict is particularly common in insects.

In our study, we wanted to understand how females adjusted their allocation of resources between survival and reproduction in different possible mating scenarios. Specifically, we assessed whether waiting for a better-quality male could be a better strategy than mating with a worse-quality male earlier in life. We used house crickets since this is a scenario that females of the species are likely to encounter and we could use size as a proxy for male quality because male size is positively correlated with beneficial genes and female house crickets consistently prefer larger males.

Cricket 2
Photos by Sean Walker

We simulated possible male-female mating scenarios by pairing either a small (< 0.30 g) or large (> 0.34 g) male cricket with a young (14-16 days), intermediate-aged (24-26 days) or old (34-36 days) female. Data were then collected on reproductive investment for the remainder of each female’s life. This allowed us to analyze differences in how females allocated resources between survival and reproduction by measuring things like lifespan, how many eggs females laid over their lifetimes and how rapidly they laid eggs after mating.

In line with life history trade-offs, we found that female age at first mating was important for how females allocated resources to survival versus reproduction. Females mated at a young age produced the most eggs but had the shortest total lifespans. Females mated at older ages produced fewer eggs but had longer total lifespans. This means that if females choose to postpone reproduction, they will not be able to produce as many offspring and fewer of their genes will be in the next generation’s gene pool.

Egg-laying rate gave insight into the physiology of why this trade-off between survival and reproduction was likely found. Old-mated females produced eggs very rapidly, but also died much sooner after they were mated. We expect that this pattern was observed because of how females produce and store eggs in preparation for mating. By the time crickets reach about 18 days of age, they have created nearly all the eggs their bodies can store and are just waiting to fertilize those eggs before they bury them in the ground to incubate. Thus, older females had to store eggs for many days, which is costly because it squishes their digestive tract and reduces their ability to take in nutrients. Once old females were mated, they would benefit from laying eggs at a higher rate. An additional limiting factor is that females can’t generate new eggs if they are already storing large numbers of eggs.

Lastly, we found that males were manipulating females to suit their own interests. Females paired with small males had shorter lifespans and higher egg-laying rates, but they did not produce more eggs overall. This means that small males manipulated females more than large females. This pattern is opposite the one found in other insects: Others have found that large males manipulate females more, which means male house crickets may use unique reproductive tactics. We expect that females were manipulated by males using a group of proteins called prostaglandins, which are found in the seminal fluids of several species including both crickets and humans. Prostaglandins are needed to stimulate females’ egg-laying and higher doses of these proteins causes females to lay eggs faster. Thus, small males likely transferred more prostaglandins, which suggests that small male house crickets attempt to compensate for their poor quality by manipulating females to lay more eggs that contain their genes.

This study describes an exciting set of interactions between female mate choice decisions and male manipulation that can have effects that last across generations. Even though females that postpone mating produce fewer offspring, the decision to wait to mate with a genetically higher-quality male could still be the better choice because females will face less manipulation from better males and will produce offspring that have better genes and are themselves more likely to pass on more of their genes. Future work aimed at describing the underlying physiology of these life history patterns and others will help further our understanding of how individual decisions can shape evolution.

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