He’s Having a Baby!

Image copyright Carin Bondar, 'The Nature of Human Nature'

It’s a common topic of conversation among new (human) mothers:  how our population would cease to exist if males had to bear the children.  The physical costs (including a 9 month gestation, followed by giving birth to a 6-10 pound live young) are extremely daunting and may not be as readily undertaken even if the physiology of the human male permitted it.  It doesn’t end there.  The duties of lactation and child care are generally responsibilities of the female parent, and such tasks involve a great deal of time and energy that could otherwise be spent creating more offspring to represent us in future generations.  Human males seem to have it pretty good: biologically speaking they, like the majority of males in the animal kingdom, contribute little more than genetic material to their offspring.  Although it may at first seem as though males get off easily when it comes to their ability to contribute to future generations, it’s not all fun and games.  Males almost universally compete with each other for sexual partners (and in many cases this leads to the evolution of elaborate physical structures, coloration or behaviors¹).  In addition, the mere contribution of sperm to the reproductive tract of a female does NOT guarantee that a particular males’ seed will be the successful fertilizer (see ‘Artifical Insemination’).  So both males and females have their own difficulties when it comes to procreation, although without question the human female would argue that her male counterpart would not be willing to do the child rearing in her place.  Do any females in the animal kingdom have it figured out a little better than us?

Enter the family Syngnathidae, commonly referred to as pipefishes and seahorses.  These fish are ‘sex-role reversed’, which means that males take on the pregnancy and childcare role and females experience more intense competition for mates.  Females deposit their eggs into a males’ brooding pouch, and he is therefore guaranteed paternity once he fertilizes them².  The brood pouches found in different species are categorized from simple membranous egg compartments on the males’ ventral side to fully enclosed brooding pouches with placenta-like structures³ (aka male bellies).  The ‘pregnant’ males take on the duties of osmoregulating the environment within the brood pouch, aerating the eggs and providing nourishment.  However, females don’t get off without some investment of their own.  They are faced with an interesting conundrum when it comes to competing with each other for mates: egg production is still required (which has a high energetic cost, unlike the metabolically cheap sperm production), so females do not have the same energetic freedom as males do when it comes to producing expensive sexual ornaments.  If such ornaments are produced, they are done so at a potential cost to fecundity, which could make them less attractive to potential mates⁴.  So what can a female sygnathid do to increase her chances to fill a males’ brood pouch?  Although they are not as bizarre as structures seen on males in traditional sex roles, females do develop reproductive ornaments that are used both to attain mates and to deter other females⁴.  In addition to the reproductive ornaments, females busy themselves with attempts at ruining the reproductive efforts of other females.  ‘Mating disruption’ occurs when large females swim in between a male and female pair while they are mating (how rude!), effectively ending the transfer of eggs⁵.  Large females are effective ‘mating disrupters’, and they have also been shown to influence the behavior of smaller females through intimidation.  The mere presence of larger females has been shown to interfere with and substantially decrease reproduction in smaller ones⁵.

So the overall conclusion is this: when it comes to syngnathid fish males are choosy and females are competitive.  Perhaps it’s just the human in me but I feel like all that competing is rather undignified female behavior…it simply isn’t lady-like to disrupt a couple in the throws of passion (or egg transfer)!  Although child rearing and care are difficult jobs (and I maintain that the human population would cease to exist should the sex roles be reversed in our species), I think that it is more empowering to be the one who chooses.  No offence to all you males out there, but if we (females) are going to do all the work to rear and care for your offspring you’d better be prepared to compete for our affections.

¹Darwin, C. (1871). “The descent of man and selection in relation to sex.” Murray, London.

²Jones, A. G., G. Rosenqvist, A. Berglund, and J. C. Avise. 1999. The genetic mating system of a sex-role-reversed pipefish (Syngnathus typhle): a molecular inquiry. Behav. Ecol. Sociobiol. 46:357–365.

³Wilson, A.B., Ahnesjo, I., Vincent, A.C.J. and Meyer, A. 2003. The dynamics of male brooding, mating patterns, and sex roles in pipefishes and seahorses (family Syngnathidae). Evolution 57: 1374-1386.

⁴Berglund, A. and Rosenqvist, G. 2003. Sex role reversal in pipefish. Advances in the study of behavior 32: 131-167.

⁵Berglund, A. 1991. Egg competition in a sex role reversed pipefish: Subdominant females tradereproduction for growth. Evolution 45, 770-774.

Sibling Rivalry at its Worst

Image Copyright Carin Bondar, 'The Nature of Human Nature'

First born offspring have it pretty good.  Mom is generally healthy and well-rested (having no other children to look after during her pregnancy), and the newly emerged micro-human has the exclusive attention of both parents and quite likely some grandparents as well.  The first born doesn’t have to share the resources of his/her parents like second and third children do.  Being a mother of three children, I think about this quite often.  I feel kind of bad for my youngest child, who gets dragged around to preschool, music lessons, play-dates and the other endeavors of his older siblings.  He inevitably gets his toys snatched away or his snacks devoured before he can get to them…and really there’s not a whole lot that can be done to change that.  A major difference between humans and many other animals with respect to sibling competition is this: first born offspring often attain independence before further offspring are born, leaving the parents to care for only one infant at a time.  This is certainly not the case in our species, where offspring remain dependent for too long for mothers to wait for independence between them (our physiology just won’t allow for 18 years between children!).  Instead, sacrifices are made and a lower amount of parental care is provided to all siblings.  So why not just have one offspring and avoid the need to sacrifice any kind of parental commitment?  This could be risky…if all reproductive effort is placed on a single offspring, and (for whatever reason) said offspring fails to reproduce, your biological fitness is doomed.  The ‘bet-hedging’ strategy¹ has been coined to account for uncertain conditions in the future: there are clear advantages to having more offspring but providing a lower amount of parental care to each.

Other (non Homo sapiens) mammals face a similar conundrum when it comes to repeat child rearing when the first offspring is not yet independent.  Fur seal and sea lion females rear a single offspring at a time, and nurse it exclusively for a period of 2-3 years.  However, many females give birth to another offspring during this nursing phase.  A long term study of Galapagos fur seals (Arctocephalus galapagoensis) and sea lions (Zalophus wollebaeki) addressed the potential conflict between siblings competing for their mothers’ resources, and also the conflict between mothers and offspring (i.e. which offspring should she nurse?  In what situations should she choose the juvenile over the newborn and vice versa?²).  Between-sibling conflict was found to be especially strong when resource levels were low, and the older sibling was unable to forage effectively on its own (away from the supplementation of the mother’s milk).  During El Nino years, (resulting in low ocean productivity) a high level of between sibling conflict was documented, which often resulted in the continued nursing of the older juvenile and the death (by starvation) of the newborn.  However, during periods of high resource availability mothers aggressively defended their newborns against the juveniles’ attempts to nurse.  You might find yourself wondering: why should a female continue to reproduce when there is a chance for her newborn to starve or when her juvenile offspring is not ‘ready’ to stop nursing?  The fluctuating conditions of the Galapagos make it impossible for the adult females to predict what is going to happen, making a bet hedging strategy important.  If food resources are plentiful when a new pup is born, it makes sense for the mother should defend the younger offspring from aggressive attacks from the older one (i.e. get off my boob and go forage for yourself, there’s plenty of food out there).    However, if food resources are scarce, the mother is expected to allow the intimidation (and starvation) of the younger sibling since the older one has already received more of her resources and is more likely to survive to adulthood.  Although the death of a pup is a high price to pay for a miscalculation in available resources, the mother still gets one healthy offspring when times are bad and has the potential for more when times are good.

The Galapagos study shows that bet hedging is an effective reproductive strategy when environmental conditions and resource availablity are unpredictable.  Over the course of her reproductive lifetime, a female seal or sea lion can maximize her overall fitness by bet hedging rather than by waiting for favorable conditions.  Humans on the other hand, have taken a lot of the unpredictability out of our ability to attain resources, so our need for bet hedging is reduced.  While an El Nino year might affect the availability of jack tuna in the fresh seafood section of the grocery store, it really has no bearing on whether there will be enough food to go around.  Although at times my youngest child has to fight a little harder for his share of resources, starvation is out of the question.  Taking the nature out of foraging has its advantages.

¹Mock, D.W. and Forbes, S. 1995. The evolution of parental optimism.  Trends in Ecology and Evolution 7:409-413.

²Trillmich, F. and Wolf, J.B.W. 2008. Parent-offspring and sibling conflict in Galapagos fur seals and sea lions.  Behavioral Ecology and Sociobiology 62:363-375.

Parents who play favorites – all’s fair in the animal kingdom…

Image Copyright Carin Bondar 'The Nature of Human Nature'

As parents, most of us vow to keep things equal between our offspring.  In theory there should be an equal amount of time investment into Suzie’s piano lessons as there is into Bobby’s tennis practice.  However, in reality these things are never quite equal are they?  Bobby’s tennis practice is across town, making the investment into his achievements larger than when Suzie walks over to the lady down the street for her piano lesson.  Next, the inevitable:  Suzie hates piano but Bobby looks as though he’s heading straight to the Olympic trials with his perfected backswing.  Resource allocation into the two offspring is suddenly a far cry from 50:50.  As humans we may say that we make equal investment into each of our offspring, this is an almost impossible task in the animal kingdom.  An additional complicating factor is this:  what about offspring with different fathers?  Perhaps Bobby was destined to be a champion based on the fact that his biological father is an admirable member of society and a physically fit athlete himself, but poor little Suzie was the outcome of a one night stand after a few too many cocktails with a character whose name you’d rather erase from memory.  Life history theory predicts that maternal investment into offspring should reflect the likelihood of said offspring to contribute to the fitness of said mother…which could be bad news for Suzie.

Many species in the animal kingdom mate with different partners in different mating seasons.  Based on a number of environmental, physical and random factors a female may not always end up with the mate that she most desires.  However, offspring are the inevitable result and so an interesting conundrum presents itself:  invest equally in all offspring despite the sub-optimal paternity of some?  Biologically speaking the answer should be a resounding no!  According to the ‘differential allocation hypothesis¹’, females of many species do not contribute equally to the health and well being of offspring sired by fathers of different quality.  In experimental mating research on mallard ducks (Anas platyrhynchos), researchers paired individual females with both high ranking and low ranking males in order to investigate whether they would invest differently in their offspring based on the identity of the father².  Egg size is entirely determined by the female, and is a critical trait influencing fitness in birds: larger eggs produce larger chicks that have an increased chance of surviving to adulthood.  Sure enough, it was demonstrated that eggs are significantly larger when females mate with a high ranking male.  Invest equally in all offspring?  I think not!

Blue footed booby (Sula nebouxii) males have a clear signal to show females that they are highly fit and ready to sire the next generation: their feet.  Female boobies prefer males with bright blue-green feet, and will actively discriminate against males without this characteristic.  Once copulation has occurred, the female generally lays two eggs, the second approximately 4 days after the first.  Both parents incubate the clutch and raise the young together until they are ready to leave the nest.   In an experiment designed to assess differential allocation hypothesis, researchers painted the feet of the male partner to a dull (unattractive) color just after the first egg was laid³.  As a result of this change in the males’ foot morphology, the second egg laid by the female partner had a lower volume as well as a lower hormonal content.  So perceptive is the female blue footed booby that within a few days of her mate quality being ‘lowered’, she reacts accordingly in her egg investment!

The effects of partner ‘attractiveness’ do not end at the physiological stage of egg-laying.  It has been shown for Zebra finches (Taeniopygia guttata) that the amount of post-natal parental care (by both mothers and fathers) varies with partner quality as well.  Parental care activities like nest maintenance, watching over young offspring, and time spent brooding, feeding and grooming them are generally performed by both Zebra finch parents; however, levels of all aforementioned activities are lower when a partner has an unattractive mate⁴.  It’s as if parents are reluctant to place all of their reproductive resources into a set of offspring that may have mediocre genes…tough luck for said offspring!

I suppose most human parents would argue against application of the differential allocation hypothesis in our species….and in many cases this would be with just cause.  Most Homo sapiens do an admirable job of investing equally in their offspring. There are many parents out there raising children that are not only born of ‘unattractive’ parents, they are being raised by parents that are not even biologically involved (adoption/foster parenting).  Despite the fact that at times Bobby’s tennis talents may overshadow the accomplishments of his sister, as a human offspring Suzie is quite likely to be well provided for.  Perhaps the animal kingdom could learn a thing or two about the importance of the nurture part of ‘nature vs nurture’ argument.

¹ Burley N. 1986. Sexual selection for aesthetic traits in species with biparental care. American Naturalist 127(4):415–445

²Cunningham, E.J.A. and Russell, A.F. 2000. Egg investment is influenced by male attractiveness in the mallard.  Nature 404: 74-77.

³Dentressangle, F., Boeck, L. and Torres, R. 2008. Maternal investment in eggs is affected by male feet color and breeding conditions in the blue-footed booby, Sula nebouxii.  Behavioral Ecology and Sociobiology 62: 1899-1908.

⁴Burley N. 1988. The differential allocation hypothesis: an experimental test. American Naturalist 132:611–628