Published 2021
THE LIMITATIONS OF TRADITIONAL ECOLOGICAL DATA AND THE NEW POSSIBILITIES IN MOLECULAR ECOLOGY
Historically, ecological research has been conducted in laboratories or in the field where phenotypic data is obtained through the observation of organism physiology, behaviour and morphology (Freeland et al., 2011). This type of data has provided information leading to some of the most important ecological theories in history. For example, the variation in beak morphologies observed by Darwin in the Galapagos finches assisted the development of his theory of adaptive radiation (Beer, 2008). Laboratory work can bestow particularly interesting information as it allows organisms to be subject to controlled conditions which scientists can manipulate according to factors of interest (Freeland et al., 2011) e.g. changing the texture of the surface which terrestrial isopods walk on and observing their behavioural response (Anselme, 2013). However, phenotypic data can be limited in providing robust answers to research questions as the phenotypes of individuals are subject to change by their environment, a process known as phenotypic plasticity (Stearns, 1989). This is significant when observing organisms in laboratories and captivity because the conditions which animals experience in these environments can be very different than that of their natural habitats and as a result, phenotypic changes in organisms can occur very suddenly (Jones & Bryne, 2017). Furthermore, phenotypic plasticity has also implicated knowledge which is significant to conservation efforts by misidentification of species or inaccurate estimates of biodiversity in natural populations (Belton et al., 2013).
Phenotypic plasticity means that phenotype may not be synonymous to genotype (Beebee & Rowe, 2004) and so argument may arise between genetic and phenotypic aspects (Belton et al., 2013). For instance, when the genetic variation between two individuals is great enough to define them as separate species, but morphologically they are identical, which species concept should be accepted? This argument may have first arisen in the 1970s, when studies using protein allozymes exposed a vast amount of genetic variation that was greatly underestimated by many scientists beforehand (Allendorf, 2016). Various DNA segments have since been used as genetic markers, producing data to add to our understanding of the ecology and evolution of organisms from the individual to population level. Namely, single-nucleotide polymorphism (SNPs) have been used to indicate loci which affect the fitness of individuals (Durham et al., 2014) and microsatellite loci have been used to detect bottlenecks in populations (Williamson-Natesan, 2005). The appropriate molecular markers can be chosen for studies based on factors such as cost, study design, material available and the type of organism in question (Zarowiecki et al., 2007). In the 1980s, highly polymorphic minisatellite DNA fingerprints became available and these could be used in the allocation of parentage by exclusion and maximum likelihood methods (Wetton et al., 1987; Miller et al., 2003). Relatedness between individuals and their reproductive success could be understood through this methodology and further, it became possible to determine heritable traits, including behavioural traits, which may evolve through modes of selection (Beebee & Rowe, 2004).
GENETICS IN BEHAVIOURAL ECOLOGY
Mating Systems
Mating systems have traditionally been recognised through observation of animal behaviour and defined by the relative number of sexual partners of each sex (Beebee & Rowe, 2004). Observation alone is restricted to telling us so much about these systems e.g. sighting every copulation event is incredibly difficult in species which have prolonged breeding seasons or cryptic mating behaviours (O’brien et al., 2018). Genetic analysis can entirely overcome these limitations and assign accurate parentage through DNA fingerprinting analysis, telling us exactly how many mothers and fathers contributed to a clutch. In some cases, the observed mating systems are confirmed by genetic analysis. This was true for the Californian mouse which socially, exhibits life-long exclusive pair bonds, a monogamous mating system where one female mates with one male (Ribble & Salvioni, 1990). DNA fingerprinting analysis disclosed the species was also genetically monogamous as only offspring sired by the parents of pair bonds were present in their litters (Ribble, 1991). Equally, many of the observed behaviours do not reflect the genetic outcome and this is where parentage by genetic analysis transformed our understanding of mating systems. Specifically, the discovery of unexpected sires has altered our understanding of monogamous mating systems.
Extra- Pair Paternity in socially monogamous mating systems
Monogamy has been considered as the most frequently occurring social mating system in birds (Ptak & Lachmann, 2003) and is strongly associated with biparental care. It is thought to be common in birds due to the nature of rearing their young and the ease with which either sex could contribute to incubating eggs and bringing the young food (Freeland et al., 2011). Furthermore, offspring survival may be much higher in species with biparental care and therefore this could explain why monogamous pair bonds would evolve (Wittenberger & Tilson, 1980; Gubernik & Teferi, 2000). However, one of the first studies using minisatellite DNA fingerprinting found that clutches of socially monogamous house sparrows contained offspring sired by males outside of the breeding pairs, the occurrence of extra-pair paternity (EPP) (Burke & Bruford, 1987). Since then, genetic studies have reported EPP in over 300 bird species (Brouwer & Griffith, 2019) as well as other taxa with biparental care such as socially monogamous beetles (Dillard, 2016) and tree shrews (Munshi-South, 2007), revealing genetic mating systems which were much more promiscuous than previously thought.
The differences found between social mating systems (the observed behaviours) and the genetic mating systems (determined from actual biological relationships between parents and offspring) means that they are now considered as distinct from one another (Freeland et al., 2011) and are related as such: that parentage assignment indicates the genetic pay off of the observed behaviours (Hughes, 1998). And so, genetic mating systems can give more insight into why social mating systems might have evolved. To demonstrate, a study on socially monogamous tree shrews using genetic parentage analysis, showed that half of the males which sired extra-pair offspring had no known behavioural mates, suggesting that males which cannot mate in a behaviourally monogamous pair may increase their reproductive fitness by pursing EPP instead (Munshi-South, 2007). EPP therefore means that males can still achieve reproductive success without forming a pair bond (Freeland et al., 2011). This can be evolutionarily beneficial for the EPP male in multiple ways, since not only is he increasing his own reproductive fitness, he also doesn’t have to waste energy on the care of his young. Better still, the male in the social-pair bond is likely to care for and increase the survival of EPP offspring (Griffin et al., 2013). These factors would explain why males using EPP have been selected for in evolution.
On the other hand, this scenario means that socially pair bonded males are at a reduced fitness when providing parental care to clutches which contain unrelated young (Freeland et al., 2011) and leads to question why males using this strategy have not been entirely outcompeted by EPP males. Genetic studies involving parentage analysis in combination with observed parental behaviour have provided some insight to this by suggesting that pair-bonded males are able to recognise unrelated offspring and reduce parental care accordingly (Neff & Gross, 2001). Additionally, evidence that the two strategies are at an evolutionary arms race has been found in biparental fish as there is indication that a lack of paternal defensive care is an evolutionary response to high paternity loss (Zimmermann et al., 2019). Similarly, in penduline tits a trade-off between the two strategies is evidenced by higher rates of EPP correlating to lower levels of paternal care (Ball et al., 2016). Overall, the evidence provided by this research proposes that there is potential for pair bonded males to adapt to challenges generated by EPP males and this, in combination with previous understandings of the benefits of monogamy, explains why socially monogamous males have persisted.
CONCLUSIONS
Genetics has enabled a significantly deeper understanding of many ecological concepts and has allowed studies to overcome the limitations of traditional observation-based methods. These methods are limited by phenotypic plasticity and the restrictions of lab or field settings. These limitations are prominent in the traditional study of animal behaviour through observation alone. In behavioural ecology, our understanding of animal mating systems has significantly benefited from the involvement of assigning parentage by genetic analysis. This has revealed entire subsets of genetic systems, such as extra pair paternity, which we were previously unaware of. In combination with behavioural observation, genetic parentage has also contributed to a deeper understanding of the evolution of social mating systems and why certain behaviours have been favoured by selection. The use of genetics has come to span across a wide range of other ecological disciplines such as conservation, taxonomy and so on, providing many new possibilities in addressing questions posed from the individual to population level. As the variety of genetic markers that become available and their uses continues to expand, the information which they provide will continue to benefit our understanding of and approaches to ecological problems.
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