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SUMMER 2005
Love is the Answer
by Judy Purdy

In the animal kingdom’s perennial battle of the sexes, the prize is the fitness and survival of one’s children.

Offspring fitness and survival — and quite possibly an entire population’s evolution — ride on the outcome of the high-stakes wager of mate choice.

“Both sexes have a vested interest in controlling reproduction,” according to evolutionary ecologist Patricia Adair Gowaty. Wild animals display not just cooperative behavior but also an arsenal of inherited courtship behaviors to coerce, resist, manipulate or deceive prospective suitors and competitors. The resulting genetic combinations equip or doom the next generation’s efforts to thrive and multiply.

In experiments with birds, insects, mice and fish, Gowaty and her international collaborators have shown that when both mom and dad win the chosen partner, the couple produces higher-quality young who themselves are more likely to survive and become parents. “Not everybody gets to be with the one they love, and reproduction with the one you don’t love is associated with a significant deficit in offspring viability,” said Gowaty, a University of Georgia Distinguished Research Professor.

And more than likely the best partner is not the quintessential, obvious heart throb. “I’m talking about a self-referential mate choice,” she said, “not a most-preferred male that all females like, or vice versa.”

Gowaty has proposed two theories to predict the consequences of mate choice. Her constraints theory says that moms and dads bear less-fit offspring when one or both must settle for a less-desirable partner, are coerced into a partnership or are simply unlucky in love because of social or ecological circumstances. Her compensation theory posits that parents caught in unfavorable, or “constrained,” unions try to compensate for their young’s relatively poorer fitness compared with other offspring. Constrained parents might lay larger eggs or deliver more sperm so as to produce more or better young in an effort to keep pace with neighbors who win their “most-preferred” partners. When neither parent gets a preferred mate, Gowaty speculates that these constrained couples might actually cooperate more as parents.

The promise of promiscuity
During three decades of research on bluebirds, mostly in rural South Carolina and Georgia, Gowaty has found that their family life is not always as harmonious as it appears. Early on she decided to investigate whether nesting bluebirds were sexually monogamous. “There was tension in that question, as you might imagine,” she said. “Many people believed that birds didn’t mess around.”

When she and her team conducted paternity tests on bluebird nestlings, they hit “pay dirt,” she said: Some chicks had DNA that aligned with mom’s DNA but not with that of her nesting partner.

As many as 20 percent of nestlings in Gowaty’s field sites are sired by one father and raised by another, contradicting scientists’ previous estimates that in 90 percent of socially monogamous songbirds, females were sexually monogamous. Within a decade of Gowaty publishing her findings, other scientists were estimating that female sexual monogamy occurred in just 10 percent of those species. (See bluebird sidebar on page 37.)

As Gowaty pondered the effects of females seeking extra partners — what scientists call “extra-pair paternity” — she saw potential evolutionary advantages. For one, a songbird mom who mates with multiple partners could broaden genetic variation among her nestlings. The greater the genetic dissimilarity between mom and a partner, the greater the possibility that young from that union will be better equipped genetically to withstand attacks from pathogens and parasites, for example. And that ultimately could spell the difference between life and death among step-siblings. Additionally, while some male sexual partners could lead to higher innate fitness in offspring, others might offer better parenting behaviors that could increase nestling success.

At that time, scientists generally considered male behavior patterns to be the primary determinant of a couple’s success and survival. But Gowaty reasoned that if female behaviors have effects on fitness, such as the number of kids produced, they also could influence natural selection. In 1994, she voiced her ideas — most of them not previously entertained by other scientists — at an international ecology meeting. The response was a buzz of skepticism. Undeterred, she organized a symposium to explore the interface between feminism and evolutionary biology and to examine evolutionary consequences of male and female behavior. Seizing the opportunity to develop a “more inclusive evolutionary biology,” Gowaty compiled a diverse collection of papers and essays — some from the symposium and others in response to it — for the book Feminism and Evolutionary Biology, published in 1997.

Gowaty also became even more convinced she must show that both sexes contribute to natural selection through mate-choice behaviors. However, she faced a problem of numbers: Polygamous males can sire many families during a breeding season, but females lay about the same number of eggs regardless of how many partners they have. How would female and male mate choice make an evolutionary difference?

As 1994 drew to a close, she had the answer: Forget about the number of offspring and find out whether mating with a partner of choice affects offspring quality. “At the time, I didn’t know the answer and nobody else did either,” Gowaty said. And to get it, she would need something other than bluebirds. She needed a wild, and therefore genetically diverse, creature that matures quickly and thrives under laboratory conditions. The lowly but serviceable fruit fly seemed perfect. For advice on raising these diminutive insects, she turned to Wyatt Anderson, a UGA Distinguished Research Professor of Genetics, whose fruit-fly genetics studies had spanned more than three decades.

Preferred mates breed success
Given that her initial ideas on mate constraints arose from females’ social limitations — being guarded by a male partner or coerced into copulation, for example — Gowaty wanted to test female mate choice only. She envisioned experiments — pairing females either with males they liked or males they didn’t like — to investigate if there were fitness variations in the young. But Anderson gently insisted they also test male choice, which itself might be insufficiently characterized. Both researchers would later see the wisdom of this approach.

First the researchers had to find out if both sexes indicate mate preference. They randomly paired virgin females with virgin males, put each couple into a “mating arena,” videotaped the interaction and then analyzed each fly’s behavior.

“The flies didn’t really tell us who they liked,” Gowaty said, “but they behaved in certain ways that allowed us to infer whether they liked each other. One way in which a passionate, ardent female indicates this, for example, is to go still.”

Hundreds of observations later, the team announced that both sexes in two fruit-fly species displayed ardent and discriminating behaviors — findings that contradicted earlier accounts of fly courtship.

“I’m guessing that earlier observations were done under a microscope with flies in very confined spaces,” Anderson said.

The research team — which included students and post-doctoral fellows — randomly assigned virgin flies to one of four matchmaking possibilities. The ideal match — mutual attraction between the female and male — was considered unconstrained. Constrained matches included: a preferred female and non- preferred male; a non-preferred female and preferred male; and a non-preferred female and non-preferred male.

To make the mate-choice criteria more rigorous, team member Yong-Kyu Kim, a UGA behavioral geneticist, modified the mating-preference arena to better fit the experimental conditions for subjected flies. His arena, made from flexible, clear tubing, allowed a chooser to see and smell two potential mates or to completely avoid one or both suitors. The arena also eliminated interaction — competition, posturing or intimidation — between the two candidates. For a mate to be considered preferred, the chooser had to select him or her twice, spending at least 60 percent of the time near the preferred mate.

“About 40 percent of the time females chose the same male twice,” Kim said, “while males chose the same female about 50 percent of the time.”

To compare reproductive success among the variously matched fly couples, the team relied on Kim to direct the tedious work of counting numbers of eggs laid and hatched, measuring offspring fitness and calculating the percentage of young that survived to adulthood.

The data revealed small but noticeable differences: In ideal matches, moms laid fewer eggs and dads delivered less sperm.

“It appears that an unconstrained female doesn’t have to have as many kids,” Gowaty said. “She’s with her preferred partner and her offspring are probably more variable, which may explain why they are healthier and survive better.”

Meanwhile, though constrained moms laid more eggs and constrained dads inseminated with more sperm, their larger biological investments yielded fewer adulthood offspring.

More surprising was that mate choice among males also affected the ratio of eggs to adult offspring. “By insisting we also test male choice, Wyatt saved me from that grandest of sexist mistakes,” Gowaty said.

The researchers are now comparing long-term survival rates for constrained and unconstrained moms. “A main longevity cost for females is egg production,” said team member Beth Tyler LeBow, a UGA doctoral student. “If females are laying more eggs, you would predict they’d die sooner because egg-laying is very expensive.”

Accordingly, LeBow, who has shown that environmental stress decreases a fly’s life span, is studying how stress affects both egg production and lifespan among moms with preferred and non-preferred mates.

The researchers also are investigating offspring fitness among moms who had either one or many partners.

Jessica Laverentz, a recent UGA undergraduate, has studied offspring outcomes when a mom is mated either with the same male throughout her reproductive life or with a series of partners. Her preliminary findings show that females mated with multiple partners have greater reproductive success in that their young have higher survival rates.

Romance vs. Matchmaking
Mate choice matters for fruit flies. But what about more complex animals like fish, birds and mammals? With a National Science Foundation grant, Gowaty organized a consortium of collaborators to repeat the fruit-fly studies in mallards, house mice, pipefish and Tanzanian cockroaches.

“This was like the animal kingdom’s version of true romance versus arranged marriages,” said consortium collaborator Lee Drickamer, who spearheaded the house-mouse component. Drickamer, who has written several popular textbooks on animal behavior, heads the biological sciences department at Northern Arizona University.

Turns out that romance trumps random matchmaking: Similar patterns emerged among all consortium-studied vertebrates.

“In virtually all these studies,” Gowaty said, “offspring viability was lower when individuals were reproducing with partners they didn’t prefer.”

Added Anderson, “It made us believe that there could be something to this idea that mating-strategy behavior may be based on natural selection.”

Among house mice, for example, matches based on romance had greater odds of bearing young. “It made no difference whether females or males did the choosing,” Drickamer said. “Differences between attraction and random arrangement showed up in the sheer numbers of litters produced.”

Mouse pups born to romance-based couples survived longer, under both lab and field conditions. The pups built better nests, staked out larger territories as adults and got caught in live traps less often. Sons usually won dominance competitions and daughters had higher pregnancy rates. The findings — published in the journal Animal Behaviour (February 2000 and January 2003) — also contradict the well-established parental-investment theory, which holds that whichever sex invests more reproductive resources also is choosier about a partner.

“For the father, the only cost is sperm, but the mother gestates, lactates and has an additional care-giving period,” said Gowaty, who collaborated on the mouse studies. Yet the male subjects were just as choosy as the females.

For mallards, mate choice not only favored romance, according to Gowaty and avian endocrinologist Cynthia Bluhm, but also provided ammunition for the compensation theory: Unlike younger ducks in arranged partnerships, older moms in the same bind laid larger, heavier eggs and their ducklings were similar in size and condition to ducklings born to older moms who mated with their most-preferred drake. “First-year females didn’t (or couldn’t) compensate when mated with males they didn’t like,” Gowaty said. “Their ducklings were at a significant disadvantage.” The mallard research was published last September in Animal Behaviour. The lone exception to romance’s advantage occurred among cockroaches. All four mating combinations yielded similar results for offspring viability, according to Gowaty. While no one could explain why, she proffered one possibility: a genetic similarity among individuals in the 50-year-old colony.

“Yet this study also showed that females mated to males they did not like died significantly sooner than females mated to males they did like,” Gowaty said. “That suggests that there are significant costs to females that reproduced with males they did not like.”

Package deals
To understand the laws of attraction at the genetic level, scientists are searching chromosomes for answers, particularly chromosomes that carry genes for disease- and parasite-resistance. One important finding is that in some animals the immune-response genes — specifically the major histocompatibility complex, or MHC genes — are packaged on the same chromosomes as traits linked to mate selection. Such traits include the manufacture of pheromones, the subtle chemical “perfumes” that attract, repel or warn other animals.

These kinds of chromosomal “package deals” could help explain the molecular mechanics of sexual attraction.

Unlike most genes, which are either dominant or recessive, MHC genes are co-dominant; both are expressed. If mom passes along MHC genes that differ from dad’s, the kids inherit a wider range of immune responses and stand a better chance of surviving a broad array of microscopic invaders. But even with fortuitous immunity combinations from mom and dad, offspring are still vulnerable. Parasites and pathogens, with their life spans measured in hours or days, have a decided evolutionary advantage. They can muster up new offense tactics hundreds of times faster than their longer-lived hosts can evolve effective defenses.

“This is the classic evolutionary arms race,” Anderson said.

Scientists have borrowed a character from Lewis Carroll’s Through the Looking Glass to describe it. Just as the Red Queen tells Alice she must keep running just to stay in one place and that to get someplace else she must run much faster, the Red Queen hypothesis says that hosts must constantly evolve new adaptations to outwit parasites and pathogens. What worked for mom and dad’s generation helps protect their young when confronted with similar threats, but it may provide little protection for sons and daughters confronted with new strains of harmful bacteria, viruses or fungi.

Environment triggers behavior
Even in collaborations with husband Steve Hubbell, a UGA Distinguished Research Professor of Plant Sciences, Gowaty never strays from her mate-choice theme. The two are writing a book about mate selection and how flexible sex roles can have adaptive advantages for the fitness of individuals. Their effort was ignited when Gowaty read a 1987 paper Hubbell wrote with the late Princeton University biologist Leslie Johnson. The paper reported a mathematical model for predicting choosy or indiscriminate mating behavior independent of an animal’s gender. Mate-selection behavior in their model was based on:

• how frequently an individual encounters potential partners;
• the individual’s survival probability;
• how much time elapses for the individual between one mating and the next; and
• the differences in fitness that would be conferred from mating with alternative potential mates.

Consequently, Hubbell and Johnson predicted that both choosy and indiscriminate individuals occur within each sex.

“The paper knocked my socks off,” Gowaty said. “Their model showed that individuals can be choosy or indiscriminant, depending on the environments they experience.”

Subsequently, Gowaty and Hubbell have modified this model to account for moment-to-moment adjustments that individuals — male or female — make in choosy or indiscriminate behaviors. And this model also puts forward the idea that such flexible behaviors are induced by environmental and social factors rather than determined by fixed genetic differences between the sexes.

Gowaty said she hopes their book also will have a striking effect on how other scientists think about sexual selection and evolution, particularly the extent to which breeding individuals can adjust their mate-choice behaviors in response to social and ecological conditions. “We have the impression that everything we’re going to say in the book will be controversial, at least in some circles,” she said. “And here I thought that I’d made my most important contributions very early in my scientific career and that the rest would sort of be mopping up.”

More likely, she’s just getting started.

For more information, contact Patty Gowaty at gowaty@uga.edu, Wyatt Anderson at wyatt@uga.edu or access http://www.ecology.uga.edu/people/faculty/gowaty.htm.

Judy Purdy is director of the UGA Research Communcations Office and editor of UGA Research Magazine.