Effect of Migratory Habits in Behavioral, Physiological and Morphological Differentiation of

Vertebrates
Daniel Bustos Forero

Regular seasonal migrations by organisms such as fish, birds and mammals represent a great
challenge for the individual due to the implications of resistance to unfavorable conditions and energy
costs during the migration. Despite high energy costs, migration habits serve different purposes.
There are species that migrate to get away from extremely harsh winters or torrid summers; others
looking for a suitable place for their reproduction, or to flee from their predators; while other species
migrate to ensure sufficient amount of food to increase their survival
According to this, natural selection has molded the morphology, behaviour and physiology of
organisms in relation to migratory habits. Therefore, intraspecific variation in migratory behavior is
often parallel to morphological differentiation; that is, changes in morphology can generate parallel
changes in courtship behavior or socialization, which allows variation within the same species that,
at some point, can lead to speciation.
Likewise, the performance of migratory displacement (air, land, water) has direct effects on fitness.
Therefore, the selection is expected to act to minimize the costs of migration, which increase with
distance traveled. The dynamic theory predicts how morphological adaptations improve the
performance of displacement in migratory habits.

Birds

Vágási, Pap, Vincze, Osváth, Erritzøe & Møller (2016)

In this paper, Vágási and colleagues argues that migratory flight performance has direct effects on
fitness. Therefore, selection is expected to act on minimizing the costs of migratory flight, which
increases with the distance covered. Aerodynamic theory predicts how morphological adaptations
improve flight performance. To test these predictions, they amassed a unique dataset of 149 European
bird species and 10 morphological traits. Through these comparatives analysis and phylogenetics, it
was established that prevailing view on the evolution of the flight apparatus suggests that flight-
related morphology is evolutionarily labile. Additionally, Vágási and colleagues note that mass
adjusted aspect ratio increased, while mass-adjusted heart weight and wing loading decreased with
increasing migration distance. Their findings indicate that selection due to migration acts on wing
traits that reduce the energetic cost of transportation to increase the flight range

To summarize, they showed that some morphological traits are likely adaptations to long-distance
migration and related flight costs. Also, combining the results about the predictors of migration
distance and covariance of morphological traits suggests that selection primarily optimizes the
preservation of energy assets during long travels to increase flight range per unit energy. By their
high aspect ratio that conserves energy and moderate wing loading that generates sufficient lift,
migrants might not be subject to strong selection for large flight muscle and aerobic capacity.

Hedenstrom (2008)
In this review, Hedenstrom present some key components of simple optimality models of bird
migration and briefly discuss what the relevant optimization currency applicable to migration should
be and how birds implement optimal behaviours. This paper deals with simple optimization models
about migration; migration strategies and annual routine models of migration and moult have also
been developed using state-dependent optimization. Also, Hedenstrom proposes that the migration
syndrome includes evolutionary modifications of morphology, the acquisition of orientation and
navigation skills and behavioral adjustments in relation to ecological and external factors.

Also, long-distance migrants breeding at high latitudes face severe time pressures, which is a probable
reason why natural selection has evolved efficient behaviours, physiological and morphological
adaptations allowing the maximum possible migration speed. Optimal migration theory commonly
assumes time minimization as an overall strategy, but the minimization of energy cost and predation
risk may also be involved. Based on these assumptions, it is possible to derive adaptive behaviours
such as when and at which fuel load a stopover site should be abandoned. Likewise, the fact that
migratory birds seem to ingest and process food at their maximum capacity is itself an indirect
indication that they are time minimizers. Likewise, the energy budget of migration can be subdivided
into the actual transportation costs and the maintenance and activity costs during stopovers. This fact
permits minimize unnecessary costs during flight.

In general, sedentary birds tend to have shorter, more rounded wings, longer tails and larger body size
in relation to wing span when compared to their migratory conspecifics. In addition, the minimization
of time generates changes in behavior because it alters the rest processes, permanence in predator
sites and time dedicated to feeding.

Johnston, Paxton, Moore, Wayne & Smith (2016)

The authors expose basis for understanding the molecular mechanisms controlling this endogenous
programme can provide functional and evolutionary insights into the circannual biological clock and
the potential of migratory species to adapt to changing environments. Under naturally timed
photoperiod conditions, we maintained captive Swainson's thrushes (Catharus ustulatus) and
performed RNA sequencing (RNA‐Seq) of the ventral hypothalamus and optic chiasma to evaluate
transcriptome‐wide gene expression changes of individuals in migratory condition. They found that
188 genes were differentially expressed in relation to migratory state, 86% of which have not been
previously linked to avian migration. Focal hub genes were identified that are candidate variables
responsible for the occurrence of migration (e.g. CRABP1). Numerous genes involved in cell
adhesion, proliferation and motility were differentially expressed (including RHOJ, PAK1 and
TLN1), suggesting that migration‐related changes are regulated by seasonal neural plasticity.

Lewis, Moore & Wang (2016)

In this article, Lewis and colleagues shows that migratory passerines arriving at stopover sites show
highly variable microbiotas, which is likely reflective of the widely different habitats and foods
utilized by migrants prior to arrival. If the previous environmental conditions led to the observed
initial variability, then the microbiotas of birds should become more similar through stopover when
migrants are in the same habitat and able to utilize similar resources. During spring 2014, migratory
Swainson's Thrush (Catharus ustulatus), Wood Thrush (Hylocichla mustelina), and Gray Catbird
(Dumetella carolinensis) were captured at a site in southwest Louisiana, USA, upon arrival after
crossing the Gulf of Mexico and one-two days later during stopover. Fecal samples were collected
and the microbial communities in them were analyzed using next-generation sequencing. The
microbiotas of the majority of birds showed distinct shifts in community composition and became
more similar during stopover, with birds stopping at the site for longer periods showing more
pronounced changes in their microbiotas. These results are consistent with the hypothesis that local
food-resource availability heavily influences the microbiotas of passerines.

In general, all the birds that improved in condition during stopover showed an increase in the
abundance of the indicator Lactobacillus OTUs, whereas the bird whose condition worsened showed
a decrease. It is possible that feeding stimulated the growth of the indicator Lactobacillus OTUs as
well. Several species of Lactobacillus have been associated with weight gain in mammals and birds,
so an initial increase in Lactobacillus post feeding could further promote weight gain in feeding birds
during stopover

Bairlein & Totzke (1992)

The authors describe how migratory habits could influence the physiology of an organism. In this
case, migration of passerine populations through Sahara Desert affect the levels of hemoglobin, plasm
glucose, plasma triglycerides, plasma enzymes and blood hematocrits. Specifically, elevated levels
of plasma glucose, plasma triglycerides, plasma enzymes, and whole blood hematocrit at the desert
sites compared with the pre-migratory values indicate the higher metabolic demands of birds in flight,
and the use of body proteins during migration. Higher levels of plasma sodium and urea nitrogen in
lean than in fat birds reflect dehydration in lean birds which suffer from the lack of appropriate
metabolic water production from fat during their migratory flight.

de la Hera, Pulido & Visser (2014)

In this paper, de la Hera and colleagues explain that in migratory bird species, juveniles normally
have shorter and more rounded wings than adults. The causes of this age-specific difference in wing
morphology, however, are largely unknown. Here, they used longitudinal data collected over 3 years
from a Pied Flycatcher Ficedula hypoleuca population to assess whether age related differences in
wing morphology are a consequence of ontogenetic changes or of selection favoring birds with longer
and more pointed wings. Study provides evidence of ontogenetic changes in wing length and shape,
whereby birds grow longer and more pointed wings as they grow older. Age-dependent variation is
likely to be adaptive and may partly explain age differences in spring migration phenology and
breeding success.

Bairlein (2002)
In this research, Bairlein argues that migratory flight performance has effect on body mass of birds.
This fact due to increase in the levels of lipids into the organism. For example, many migratory birds
accumulate large amounts of lipids as the prime energy source for their long-distance flights. This fat
accumulation is mostly under endogenous control, reflecting genetically programmed temporal shifts
of the body mass set point. It is accompanied by an increase in daily food intake and food utilization
efficiency and by a seasonal shift in food selection.

Seasonal frugivory appears to play a key role in many migrants. Fruits have a high content of fatty
acids indispensable for building up the specific depot lipids. In addition, plant secondary compounds
seem to play supportive role, but the mechanisms are not yet known. This lipid accumulation
represents a mechanism for physiological adaptation to migratory habits. Likewise, accumulation of
lipids generates a change in the morphology due to require new spaces or volume increase for storage
these compounds.

Morganti, Åkesson & Pulido (2015)

In this article, Morganti and colleagues stablished that is possible that birds of different sex or age
categories have different abilities to compete with conspecifics that overwinter in the same
geographical area. For this, they studied the association between morphology and migratory
behaviour in a partially migratory Blackcap population from eastern Spain, in which individuals
belong to one of the following three migration categories: all-year resident local birds (residents),
local breeders that migrate and, therefore, are not present in the area in winter (local migrants) and
central European breeders that are present in the area in winter (northern migrants). Results show that
Blackcap population at a European scale, it could consider this ‘migrant morphology’ found in
Blackcaps breeding as intermediate, lying between the morphology of completely sedentary and
marked migratory populations. This intermediate morphotype may be maintained by natural selection
if migration in this population is facultative.

The main result of the study is that, in the partially migratory population studied, morphology and
migratory behaviour are not correlated. In many cases, this behavioral and morphological
differentiation it couldn’t be due to the phenomenon of migration. Even though, variables into the
same environment such as competition, specialization of diets, among others could be responsible to
the variations in morphology.

Fishes

Saito, Watanabe & Murase (1995)

In this article, the fatty acid composition in lipids of the muscles and other internal organs of bonito
(Euthynnus pelamis) caught in different seasons was analyzed, and in addition, that in the lipids of
the stomach contents originating from their prey organisms was also analyzed. The purpose of this
analysis is based on to evaluate the variation of concentration of fatty acid in lipids in organisms pre-
migration and organism in migration. According to results, although docosahexaenoic acid in the
lipids of the stomach contents originating from their prey organisms varied from about 13% to 31%,
it was the dominant unsaturated fatty acid and accounted for more than 25% of the total fatty acids in
the lipids of every organ of bonito in and out of season, and its seasonal variation was comparatively
small. In summary, accumulation of fatty acids in migratory organism as E. pelamis represent an
energy source during migration; also, this accumulation generates an advantage on fitness.

Jonsson, Jonsson & Hansen (1997)

In this paper, Jonsson and colleagues estimated the energy content of Atlantic salmon at different
times during sexual maturation from the proportions of protein, carbohydrate and lipid in dried
material. They observed that the annual energy loss during upstream migration and spawning was 60-
70% of the total energy content in summer. This is a minimum estimate as the fish might feed between
sampling in the fjord and in the river. Also, a large of the energy loss during upstream migration and
spawing was due to a decrease from over 11% of the body mass in summer to less than 2% of the wet
mass after spawing. In comparison, the lipid content of cultured salmon prior to maturation is 18%
and it decrease 8% at spawing. Although the reproductive investment in Atlantic salmon is high, it is
lower than that of semelparous Pacific salmon Oncorhynchus spp., which may use 80% of their total
energy during upstream migration and spawning.

In summary, the annual energy loss of adult Atlantic salmon during upstream migration and spawning
was more than 60% of the total available energy at the time the salmon were assumed to cease feeding.
Further, the cost appears to be higher in large than in small salmon. In both sexes, most of the energy
reserves used were mobilized from the muscles rather than the visceral tissue. After spawning, total
energy content were similar in females and males, indicating similar energy expenditures for the two
sexes. This energy saving and directed towards the muscles, allows an improvement of fitness by
means of physiological changes (energy saving), morphological (greater volume of muscles) and
behavioral (alteration of normal eating habits) to fulfill the purpose of migration and spawning.

Slotte (1999)
In this article, Slotte analyzes the effects of fish length and condition on spawning migration in
Norwegian spring spawning herring. According to this, the relative weekly energy loss is 3-4 times
higher during the spawning migration than during the wintering, and it increases with decreasing fish
length. Survival of progeny may increase to major fish length due to beneficial environmental
conditions. Besides, large-sized fish have higher volume for fat accumulation (energy source during
migration) and greater muscle development. These characteristics could be considered as adaptations
to migratory habits. Although, large body size increases the degree of attack by predators

Mammals

Ahlén, Baagøe & Bach (2009)

This research on migration and activities of bats at sea have resulted in information about the behavior
and distribution patterns of migratory bats, including regular occurrences of many species travelling
over open water, seasonal differences in the distribution of migrating bats, and detailed observations
of flight behavior, echolocation calls, and roosting and feeding habits of bats at sea. Eleven of 18
species occurring in the region were detected at departure points and out at sea, suggesting that
migration and foraging over marine environments are common. They show that some bat species
from the Scandinavian Peninsula no hibernate on the European continent and therefore must migrate
across large stretches of open sea.

Bats must use systems of orientation other than echolocation for long-distance navigation, but they
argue that bats migrating over the sea fly low to detect the water surface by echolocation to remain
oriented. It is also possible that lower wind speeds at the low altitudes are favored by bats. This
modification in the echolocation mechanism represent a morphology innovation for increase the
probabilities of success in migration. Also, positively affects fitness.

McGuire, Guglielmo, Mackenzie & Taylor (2012)

In this article, McGuire and colleagues document the behaviour of L. noctivagans at an autumn
migration stopover site to better understand the occurrence and significance of stopover in bat
migration. Specifically, we set out to document the timing of migration, roosting and foraging ecology
during migration, and to determine stopover duration and departure direction. Their results suggest
that migrating bats stopover for sanctuary or short-term rest as opposed to extended rest and refueling
as in many songbirds. Daily torpor could reduce energy costs when not in flight, minimizing the need
for extended stopovers and allowing bats to potentially complete their migration at a fraction of the
time and energy cost of similar sized birds.

Hausfater & Meade (1982)

In this paper, Hausfater and Meade exposes present evidence both that infective ova and larvae of
intestinal parasites are found at very high densities in the soil beneath sleeping groves and that
Amboseli baboons substantially reduce their contact with this reservoir of parasites by alternating
periods of a few consecutive nights' use of any grove with much longer periods of avoidance of that
grove. Although many factors other than the presence of parasite larvae also influence choice of
sleeping groves, they propose as a working hypothesis that the temporal pattern of sleeping grove
alternation shown by Amboseli baboons reflects a subtle behavioral strategy for parasite avoidance.
Also, this strategy for parasite avoidance could be useful for short distance migrations. Strategy for
parasite avoidance could be an exaptation for migratory habits due to increase fitness into population.

Able & Belthoff (1998)

Able & Belthoff investigated about the case of migration of house finch. The house finch
(Carpodacus mexicanus) of eastern North America was introduced onto Long Island, New York,
around 1940. The source is presumed to be southern California, where 80% of individuals are
completely sedentary. The eastern population has become migratory: by the early 1960s, 36% of
eastern house finches were performing migratory movements (more than 80 km from their banding
site) and that proportion has fluctuated between 28 and 54% in succeeding years. The movements of
birds banded during the breeding season and recovered in winter were strongly orientated towards
the south-west, and the same pattern was evident in the earliest recoveries; recoveries of birds banded
during winter and recovered in the breeding season were orientated toward the north-east. The
average distance of migration has continued to increase logarithmically. Areas colonized later, as the
range expanded, were characterized by initial long migration distances and high proportions of
migrants, suggesting that these traits have evolved in the eastern population. Eastern house finches
are partial migrants: not all individuals migrate, and birds that migrate some winters remain in
breeding areas in others. Younger birds exhibit a stronger tendency to migrate. A very few western
(including southern California) house inches moved long distances, but they did so in directions
consistent with seasonal migration, indicating that the machinery subserving migratory behaviour
pre-existed in the parent population. This case reflects the fact that migratory habits causes
behavioural differentiation between same population.

Turtles & Snakes

Courtillotl, Hulot, Alexandrescu, le Mouë & Kirschvink (1997)

This research provide evidence for remarkable sensitivity of sea-turtles to the earth's magnetic field
and suggest that it is used by these animals to determine global position and to navigate (migratory
habits) They emphasize that a consequence of these observations taken together is that sea-turtles
should be able to accurately detect the full (vector) magnetic-field, and perhaps spatial gradients. To
interpret these observations, they propose a simple model in which the turtle is considered as a small
permanent magnet, on which the geomagnetic field exerts a torque. This torque varies as a function
of turtle azimuth and field parameters which depend mainly on latitude. Although this simple model
accounts for some of the observational evidence discrepancies might be due to several other factors,
such as speed of magnetic field changes during experiments or lack of field homogeneity. Also, the
earth's field has varied significantly over the last few centuries and some of the magnetic features
observed today were very different or even not present two or three centuries ago. This would place
constraints on the rate at which genetically inherited magnetic behavioural preferences can change
with time. In summary, capability of magnetic navigation of turtles is relevant in migratory habits
due to increase the probabilities of survival during migration. Also, magnetic navigation of turtles is
an exaptation because many non-migratory turtles also have a magnetic localization system.

Madsen & Shine (1996)

In this research, Madsen and Shine documented migrations of large predatory terrestrial reptile that
follow migrating prey. They observed the system of water pythons (Liasisfuscus) - dusky rat (Rattus
colletti) in adjacent floodplain in the wet-dry tropics of northern Australia to document patterns of
movement, with emphasis on the ways in which the snakes exploit their major prey species, So, the
distribution and abundance of these rodents vary seasonally. During the dry season the rats live in
soil crevices in the floodplain, but wet-season flooding forces them to higher ground, primarily to
natural levee banks. Python and rat abundances on the floodplain adjacent to floodplain were
significantly correlated through time: both reached a maximum during the dry season and fell
dramatically during the wet season. Most pythons migrated to the vicinity of levee banks on the
floodplain up to 12 km away from their dry-season range. By migrating seasonally, water pythons
can efficiently utilize a migratory prey species that would otherwise be unavailable for much of the
year. This is the typic case where the predator acquires similarly migratory habits to prey for increase
survival probabilities

Lohmann & Lohmann (1998)

In this article, Lohmann and Lohman argues that migratory guidance mechanisms in marine turtle are
influenced by lines of magnetic field around the world. Also, sea turtles may use the earth's magnetic
field not only as a cue for compass orientation but also as a source of positional information. Results
have demonstrated that turtles as Caretta caretta can detect inclination angle and field intensity, two
geomagnetic features that vary predictably across the earth's surface. In summary, evolution of
migratory habits generates new systems of localization and dams to use the physical and chemical
resources of the environment to increase the fitness.

References

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