Naturally occurring behavioural paradoxes are prevalent when studying animal behaviour.

Although
at first they may seem to reduce an individuals fitness, through further examination it seems that
they are usually highly beneficial. In this essay, I will address the paradoxes of multiple mating’s in
females (referred to from now as polyandry), non-kin cooperation and departure from food patches
that are not fully depleted.

The paradoxical nature of polyandry, in which females have multiple mates, is widely discussed in
the subject of sexual selection. Repeated mating is costly as there is an increased risk of predation
and sexually transmitted infections, alongside an increased chance of direct harm from the male
during copulation. Needless to say, the energy expenditure is higher when there are multiple
matings (Roberts et al 2015). Despite this, polyandry is taxonomically widespread. On second
consideration, it appears the advantages of polyandry are in surplus for females. Sequential
polyandry provides the females with the choice to re-mate with a “genetically superior” male,
ultimately increasing the indirect fitness of the female as her offspring will inherit the higher quality
genes (Byrne et al 2019). Arguments for polyandry benefitting the indirect fitness of the female are
widely disputed. A study comparing monogamous and polyandrous female drosophila melanogaster
suggested that polyandry was not causal to fecundity, egg hatch rate, larval viability and
development time, and there was no significant difference between the polyandrous and
monogamous groups (Brown et al 2007). Although in many social insect species, the queen –
through polyandry – can produce colonies with extensive genetic diversity that are resistant to
disease and have “optimum division of labour”. Arguments surrounding the improvement in genetic
quality are still challenged, yet it is undisputable that polyandry will surely improve genetic diversity,
which in turn will improve fitness on a macro-evolutionary scale. Be that as it may, polyandry does
undoubtedly lessen the likelihood of unviable offspring as the more males the female mates with the
lower the possibility of mating with a genetically incompatible individual. This is the genetic
incompatibility hypothesis (Roberts et al 2015). Polyandry also promotes sperm competition and
cryptic female choice, providing the female with post-copulatory mechanisms to “screen males after
copulation” (Simmons 2001). Sperm competition is in itself an indicator of male fitness and cryptic
choice only provides the female with further choice over who sires her offspring, as she may expel
any unwanted ejaculate from undesirable mates. Admittedly, polyandry usually results in a single
parent raising their offspring, which certainly requires more energy input. However, in doing so the
risk of infanticide is effectively removed. It is inferred that in species where males usually express
infanticidal behaviour, polyandry evolved as a counterstrategy so females may conceal paternity
(Klemme & Ylönen 2009). Lastly, the most explicit reason for polyandry is simply to do with providing
a sufficient sperm supply. Modelled through Drosophila, it was shown that fecundity was largely
increased through multiple matings (Ridley 1988) and in another insect study it showed that 58% of
the insects in question were not provided with enough sperm after a single ejaculation. It is evident
why polyandry is a ubiquitous, yet variable, phenomenon throughout the taxa: it provides huge
benefits to the female, despite at first seeming illogical and inherently paradoxical.

Cooperation with non-kin in a Darwinian world of natural selection may at first glance seem
contradictory and paradoxical. Primarily, kin selection and Hamilton’s rule explains how cooperation
is mutually exclusive with relatedness: the more related two individuals are the more cooperative
they will behave (Queller & Strassman 2002). Considering the costs of cooperation and sociality -
increased competition over food, higher transmission of infection and general energy input - it does
call forth the question, in a competitive world why help another individuals kin at a fitness cost to
oneself? Albeit non-kin cooperation is widespread throughout the taxa, on the extreme end of the
spectrum lie eusocial species, this usually refers to ant, bee, wasp and termite species. Eusocial
species have a caste system in which lower caste individuals are sterile yet cooperate to rear the
young of the entire colony, produced usually by a single queen (Queller & Strassman 2003). One
explanation for eusociality is haplodiploidy where the father produces identical haploid sperm and
the mother’s egg is diploid. This creates a coefficient of relatedness of 0.75 between the siblings.
Notably this is a higher coefficient than observed between haploid offspring, therefore Hamilton’s
rule is still satisfied and largely explains eusociality. However, when the coefficient of relatedness is
as low as 0, cooperation is still observed. Reciprocal altruism wholly explains this paradox. In 1972
Robert Trivers used the term ‘reciprocal altruism’ to describe a process where individuals are
cooperative with non-relatives at a cost to themselves. Now, it is comprehensively agreed that
altruistic behaviour evolved through expectation of receiving return benefits (Waal 2008). A study
into reciprocal altruism on bats showed that food sharing was biased towards familiarity rather than
kinship. Moreover in a group of mixed relatedness captive bats, previous food donations were more
significant than kinship, when it came to food sharing or grooming, as bats were almost nine times
more likely to prioritise reciprocating donations to a previously altruistic behaving individual
(Wilkinson et al 2016). It would appear a group made up of entirely selfless altruistic individuals are
advantageous over a group of partially or exclusively selfish organisms. Yet, reciprocal altruism is
vulnerable to cheaters when there are some individuals acting entirely selfishly (Ale et al 2013).
Tactics in place to avoid assisting non co-operators have arisen through indirect reciprocity where a
third party observes and monitors interactions between the performer and the receiver (Clutton-
Brock 2009). This provides two outcomes, individuals should be more inclined to help those that
have helped others and individuals should be more aware of their “reputation” by publicly being
cooperative. However there is little evidential support behind indirect reciprocity. One example
through a recent study on capuchin monkeys showed that individuals who had recently groomed
another member did not receive an increase in grooming themselves. Furthermore, the capuchin
monkeys did not appear to share food more readily under the presence of an observer (Schino et al
2021).

An optimal forager should pursue the highest foraging efficacy attainable, meaning obtaining as
much energy per unit of time as possible. By reducing foraging time, selecting foods with high
nutritional value and low processing time and abandoning a food patch when depleted should, in
theory, provide an individual with optimal gain: this is known as Optimal Foraging Theory (OFT).
However, leaving behind a patch where resources are still available is, in appearance, less than
optimal and once again paradoxical yet is still a regular occurrence. The Marginal Value Theorem
(MVT) predicts how long an individual should exploit one patch before moving to another,
dependant on patch quality and distance to next available patch. According to the MVT a forager
should stay for as long as the marginal rate of food on a patch is equal to the average food across all
the patches (Charnov 1976). An in situ study on southern elephant seals showed that diving duration
did not increase in high quality patches, rather in low quality patches. Additionally, there was higher
descent and ascent rates in high quality patches, suggesting when quality is high foraging time is
minimised. This challenges the view that maximised foraging time corresponds to foraging success,
therein explanative of why an animal may leave resources behind at a patch (Thums et al. 2012). As
the MVT predicts that that a forager will leave a patch when the marginal rate of food is less than
the average food across the other patches, a critical assumption is that feeding rate of one patch will
decrease as animals deplete the patch. Nevertheless, it is widely observed that feeding rate and
patch depletion are not mutual to each other. A study on wild Bornean orangutan showed there was
no significant difference in feeding rates when comparing the first and last bout, the time spent on
the patch did not decrease (DiGiorgio et al. 2020). Alternatively, the Ideal Free Distribution model
(IFD) predicts that foragers will distribute themselves across patches in attempts to provide equal
gain to all individuals (Fretwell 1969). Although the IFD makes some simplifying assumptions, that
individuals have similar competitive ability and that individuals “know” the availability of resources
on all patches. Under further consideration, assuming this almost anthropomorphises the animal
and blatantly ignores the wide variation of foraging ability present in animal populations.
Disregarding these assumptions may expedite understanding the paradox of why some animals
leave a patch where resources still remain.
The behavioural paradoxes of polyandry, non-kin cooperation and incomplete food patch depletion
explored throughout may now seem less paradoxical and more understandable. Even at first an
animal may appear to be acting at a fitness loss to oneself, in a world where natural selection is the
driving force behind evolution it is usually not the case and these, so called, paradoxes mostly
adhere to the expected results of natural selection.

Word Count - 1500

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