Introducing paternal care

I recently assigned our second year evolutionary biology students the task of creating a blog dedicated to some aspect of evolutionary biology. They did an amazing job, so much so that I’ve decided to change my blogging to express a little more closely my biological interests, rather than just focusing on a particular journal article. I thought I’d start by focusing the next few blogs on one of my major interests, the development and expression of paternal care behaviour. 

So, what is paternal care? Paternal care, as defined by Dewsbury (1985) and Woodroffe &Vincent (1994), is any direct or indirect non-gametic investment that is made by the father after fertilization that either directly or indirectly benefits his offspring. Direct paternal care includes behaviours performed in the young’s presence such as huddling (e.g. Djungarian hamsters Phodopus sungorus; Fig. 1), grooming, retrieving, providing food, defending against predators, babysitting or socializing (Malcolm 1985).

            

Fig. 1 Djungarian hamster Phodopus sungorus                    

(Alalein: picture accessed 04 July 2014; 15h26)
(http://www.deviantart.com/morelikethis/artists/310003570?view_mode=2)       

Importantly, these behaviours can influence the survival, growth and behavioural and cognitive development of the young. Indirect paternal care includes behaviours performed in the absence of young, but which may still influence survival, growth and development. These behaviours can include alarm calling (e.g. California ground squirrels Otospermophilus beecheyi; Video 1), female care and provisioning and territory maintenance (Malcolm 1985).

Video 1 California ground squirrel Otospermophilus beecheyi alarm calling)

(Life at Laguna: video accessed 04 July 2014; 15h26)
(http://www.youtube.com/watch?v=RmfDbWH46bQ) 
 
While paternal care is relatively common in birds, it tends to be quite rare in mammals, occurring in only 5-10% of species (Wright 2006). Paternal care has been recorded in six mammalian orders, namely carnivores (e.g. bat-eared foxes Otocyon megalotis, Wright 2006; Fig. 2), cetaceans (e.g. killer whales Orcinus orca, Lopez & Lopez 1985), diprotodontids (e.g. rock-haunting ringtail possums Petropseudes dahlia, Runcie 2000), primates (e.g. common marmosets Callithrix jacchus, Schradin et al. 2003; humans Homo sapiens; Quinlan 2003), lagomorphs (e.g. European wild rabbits Oryctolagus cuniculus; Cowan 1987) and rodents (e.g. African striped mice Rhabdomys pumilio, Schradin & Pillay 2003; Fig. 3). 

Fig. 2 Bat-eared fox Otocyon megalotis  
(Joe & Mary Ann McDonald: picture accessed 04 July 2014; 14h32)
(http://hoothollow.com/Trip%20Report%20-%20Kenya%20Nov-Dec%202005.html)

 Fig. 3. African striped mouse Rhabdomys pumilio
 (Tasmin Rymer: personal picture)

In my next blog, I’ll focus a bit more on the evolution of paternal care.

Summary: Dynesius & Jansson (2000)

Over the course of Earth's history, climates have varied widely. Some climate cycles are reported on the scale of 10-100 thousand years, such as Milankovitch oscillation. Milankovitch cycles have been demonstrated to influence the location and size of species geographical distributions. Dynesius & Jansson (2000) further suggest that Milankovitch cycles also drive geographical patterns of species diversity, polyploidy, degree of specializations and the dispersal ability of organisms. When species ranges  are influenced by these climate cycles, they can be termed ORDs, or "orbitally forced species' range dynamics". These ORDs may constrain short-term evolutionary processes. Although adaptations may accumulate between climatic shifts, they may be lost when the climate shifts, due to population extinction of variation in selection pressure. The size of ORDs varies on both temporal and spatial scales, and can function to decrease gradual speciation, increase species range size and proportion of polyploid species. ORDs favour dispersability and tend to favour generalizations. Dynesius & Jansson (2000) indicate that large ORDs can promote species persistence (neither extinction nor speciation) and that ORDs show a corresponding increase with latitude (although how these ORDs vary with longitude or altitude is not indicated). One of the latitudinal patterns observed by ORDs is Rapoport's rule - a gradient in species' range sizes and diversity. Dynesius & Jansson (2000) argue that ORDs of different strengths may explain several biological phenomena (i.e. one driving force as opposed to many). ORDs provide a new opportunity for developing conservation strategies on different environmental scales.

Summary: Dukas & Jongsma (2012)

Female mate choice is common in the animal kingdom and females and males may come into conflict over a female's choosiness. In particular, males that are chosen less frequently by females may resort to forceful copulations in order to gain some reproductive fitness. In fruit flies Drosophila melanogaster, males may force-copulate with sexually immature females just after eclosion, a particularly vulnerable time for females. Although males only achieve approximately 20% of successful matings this way, the results for females are significant. Females suffer reduced longevity, high wing damage and show lowered reproductive success (through generation of fewer progeny, which they can still produce). Although females are capable of remating at sexual maturity after a forced copulation, mating is generally followed by a period of diminished receptivity and attractiveness, meaning that females may not be able to mate until a later time. Dukas & Jongsma (2012) quantified the effects of forced vs. consensual matings on the receptivity and attractiveness of females, to determine whether forcibly mated females are able to overcome the effects of mating by showing faster return to receptivity and attractiveness. Although forcibly mated females appeared as attractive as same-age virgins, and were more attractive than recently consensually mated females, Dukas & Jongsma (2012) found that they remated at a lower frequency than same-age virgins, but a higher frequency than recently mated females. In the case of fruit flies, it seems that males benefit through forced copulations by gaining some fitness benefits through generation of progeny. Although damaging to females, females are able to overcome this negative behaviour, and can gain matings later through return to attractiveness and receptivity (even if only partially).

Summary: Montgomery (2014)

 Many mammals, including primates, play. Play includes those behaviours that appear incompletely functional, atypical, spontaneous and repeatable, and are elicited under conditions of low stress. Play is easy to recognize, but is often difficult to define. Play is primates occurs often, although nonadaptive and adaptive explanations for its occurrence are plentiful. In primates, social play has been linked to the relative size of various brain regions, including the neocortex, amygdala, cerebellum and hypothalamus, suggesting that play is involved in the development of cognition. These structures have also been shown to be involved in the ability to first predict, and then perform, sequential actions, indicative of behavioural flexibility. Using data on the frequency of social and nonsocial play in various primates, Montgomery (2014) attempted to find evidence that could directly link play to behavioural flexibility and/or brain maturation. He found that postnatal brain growth increased with the frequency of play and that measures of behavioural flexibility are associated with the frequency of play. Montgomery (2014) concluded by indicating that the results from this study provide an adaptive framework for play.

Summary: McComb et al. (2014)

An animals' ability to perceive and recognize predators, as well as assess the threat they pose, is crucial for the survival and persistence of the individual and, by extension, the species. By assessing the threat, animals can minimise the cost of retreating if the threat is unfounded, while maximising the time spent engaged in other activities. While most small-bodied animals are faced with a variety of predator threats, larger-bodied species, such as elephants Loxodonta africana may not experience the same pressure from predation. However, elephants and other large-bodied animals are at risk of predation by humans, due to humans increased cognitive ability to hunt these larger-bodied resources. McComb et al. (2014) investigated elephant responses to vocal playbacks of different humans in Amboseli National Park, Kenya. They tested whether elephants responded differently to 1) adult male human voices from two different ethnic groups (Maasai and Kamba), 2) male and female human vocalizations; and 3) young male human voices (boys). They resynthesised the adult male vocalizations to mimic female voices. McComb et al. (2014) found that elephants used more defensive bunching postures and investigative smelling following adult male Maasai vocalizations, compared to Kamba male vocalizations, consistent with the high predation threat imposed by this group of humans. In addition, elephants were less likely to demonstrate a strong behavioural response to female and young boy vocalizations, indicating an ability to distinguish between different vocal qualities. While McComb et al. (2014) suggest that this may be a function of selection in these cognitively advanced animals, with increasing human pressure, it would be interesting to determine whether this is a more general response than expected.

Summary: Atwood et al. (2012)

Increased mortality and morbidity can result from alcohol consumption and high levels of  consumption and increased episodic "binge" drinking incidents are increasingly becoming more of a social concern. Alcohol consumption is sensitive to a variety of factors, including price, drinking age restrictions, hours/days of alcohol sale and number/density/type of alcohol outlets. Atwood et al. (2012) explored another factor thought to influence alcohol consumption - glass shape. They exposed 159 male and female alcohol consumers to either lager or soft drink (7-Up), straight or curved glass and 6 fl oz or 12 fl oz (in various combinations). Thereafter, participants completed a word search puzzle to disguise the true aim of the experiment. Atwood et al. (2012) measured rate of consumption, total drinking time, perceptual judgement of the half-way point of the glass. They found that rate of consumption decreased by 60% when alcohol-drinking consumers drank from a straight glass compared to a curved one, but this was only observed when the glass was full (12 fl oz). Atwood et al. (2012) also found that the half-way point of a curved glass was more difficult to estimate than that of a straight glass, suggesting that glass shape can influence rate of consumption of alcoholic beverages. This could be an effective strategy for alcoholic consumption management.

Summary: Pappano et al. (2012)

 Living in a group confers numerous benefits, such as reduced energy expenditure for thermoregulation (social huddling), increased predator detection (with reduced individual vigilance - the "many eyes" hypothesis) and increased predator defence (e.g. mobbing by many). Hamilton (1971) postulated that groups form because individuals are inherently selfish and grouping can diminish costs associated with living alone. Both De Vos & O'Riain (2010) and Quinn & Cresswell (2006) have demonstrated that the the central tenets of the "selfish herd hypothesis" can hold true in some mammals and birds. Pappano et al. (2012) postulate that this idea can also translate to "social predators" - infanticidal males. They proposed that the impact of a non-breeding, potentially infanticidal bachelor male geladas Theropithecus gelada, could alter spacing patterns of  reproductive units within a group. Their findings suggest that these social predators are capable of causing group spacing dynamics to change: 1) numbers of animals in a group increased with an increasing number of bachelor males; 2) breeding individuals moved into closer contact with neighbours closest to them; and 3) reproductive females associated more with reproductive males. Pappano et al.'s (2012) study indicates that spacing patterns of individuals could offset the costs of potentially associating with social predators within groups.